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To be the Brave and Imperfect Female Graduate Student

To Celebrate International Women’s Day, I decided to forgo my typical academic-esque post. I am not one for personal stories, but a recent realization has inspired me to address one particularly significant issue we ladies of academic face.

Over the last few weeks, I have noticed an unsettling pattern in my conversations, particularly with my professors. For the past two semesters I have been enrolled in two classes that have been particularly challenging for me: Geographic Information Systems (GIS) and Statistical Inferences and Analysis. Both classes have, to put it lightly, tested my patience. There were times in the GIS lab, as a realized I was closing in on hour 6 of time spent on a project, that I wondered what on earth possessed me to follow this particular career. I tend to pick up concepts quickly, be it from an innate ability to understand information quickly or just working hard. Yet, in both of these classes, that immediate, satisfying comprehension did not necessarily arrive in the timely manner I am used to. Instead I struggled. Instead I’d agonize over whether or not I was typing commands correctly in ArchGIS. I’d get frustrated when I did not immediately understand the different types of z-scores. It was not until the other day when both of these professors told me, independent of each other, that the main reason I struggled with these classes was because I was afraid of not doing the assignment perfectly.

 

This struck a cord with me, and it wasn’t a happy tune. Yesterday evening, I stumbled across a TED talk by Reshma Saujani titled, “Teach girls to be brave, not perfect,” in which Saujani discusses how woman have been socialized to aspire to perfection, and are therefore overly cautious. Saujani cites studies of fifth graders found that the more intelligent the girls, the more more likely they were to give up on a difficult assignment, while the more the intelligent the boys, the more likely they were to meet the challenge. Young girls were more afraid of showing their imperfection while attempting to complete the assignment. Saujani says women do not necessarily suffer from a lack of confidence, but it is this socialization of perfection that causes women to take less risks in their careers. If women were socialized to be brave, rather than socialized to be perfect, that could move society forward.

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All graduate students already, shall we say, encounter a daily  crisis-of-self (or maybe that’s just me). Be it from coursework, grant writing, or just the ongoing battle of “will-I-get-a-job-that-isn’t-at-a-banana-stand?” saga (though there is always money in the banana stand), I think there is an additional issue that plagues graduate students, particularly females. I think that many of us were (and continue to be) socialized to strive for perfection.Why are we so concerned with being perfect? Wouldn’t it be more useful for our academic careers to be socialized to take risks, to be unafraid of failure, to be brave?

During my classes, I notice that females are not particularly vocal in class. Maybe we don’t speak out in class because we don’t want to sound unintelligent. In her insightful guest blog for “The Professor is In”, Karen Cardozo also explores this topic, noting that women take fewer chances and risks than men. “For example, in test-taking studies, researchers found that upon closer inspection, perceived gender differences in performances resulted not from wrong answers, but from women’s greater tendency to leave an answer blank when unsure about it (thus eliminating even partial odds of hitting upon the correct answer).  When the experiments were revised to insert the instruction “do not leave any answers blank,” there was no gender disparity in performance.” Furthermore,  studies have shown that males tend to dominate classroom discussions compared to females, possibly because, “women prove to be extremely vulnerable to interruption. Numerous studies have demonstrated that in mixed-sex conversations, women are interrupted far more frequently than men are…Moreover, once interrupted, women sometimes stayed out of the discussion for the remainder of the class hour.” While, luckily, my male peers do not interrupt my female colleagues, I should point out that in order to change the socialization of perfection into bravery, it will take the efforts of both females and males.

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Since I began applying for graduate school, I had multiple professors (all female) ask if I applied for external funding, specifically the NSF. Thinking that I was not qualified, or worse yet, that I would devote all this time to apply and therefore put myself in the position of possibly failing, I didn’t bother. It was not until last fall when I was reading advice on how to write a successful NSF application, did one of my professors (once again, female), ask me what I was reading, and then inquire why I wasn’t applying for the NSF. It is absurd that I talked myself out of applying so many times. It was the encouragement from my female professors and colleagues that drove me to apply for the grant last fall. It took someone explicitly telling me that yes, I am qualified, and even if I weren’t, I should apply anyway.

Regardless of the outcome, I think having the courage to apply for these grants is a personal success. Unfortunately, women are less likely to apply to major grants.  While the social sciences have noted that women are beginning to be more fairly funded in the social sciences (specifically in the UK), there are still issues in gender balance of how many women apply for grants, and the percentage of them who receive them. Similarly, in the job market, Saujani notes that men are likely to apply for jobs when they meet approximately 60% of the requirements, while females only apply when they meet 100% of the requires. With these discouraging numbers, it’s no wonder that women think we cannot apply for grants because we don’t have enough publications, experience, or simply don’t want to risk failure. We need to change the perception of perfection: socializing women to think they are only valuable if they are perfect hinders us more than it helps us.

So in order to remedy this whole socialization of perfection, I think we, female academics, need to socialize our colleagues and peers in the process of being brave. Those of us who spend our field seasons working in deserts, rainforests, and mountains littered with poisonous snakes, bugs, plants, basically all manner of creatures that could harm us, may disagree: to do these things does require bravery. What I am talking about is having the bravery to take risks in our careers. We need ignore that pesky and unproductive manta, “I may fail at this, if I do, I’m not perfect,” and instead replace it with, “I may fail at this, but oh well, I was brave for trying.” To achieve this, it will take a concentrated effort for all of us, fellow female peers and colleagues, not to mention male peers and colleagues, to encourage bravery, and show that perfection is overrated.

On a final note, public outreach is an invaluable tool academics can use to encourage the next generation of women to be brave, so show how perfection is harmful. This past weekend, in collaboration with GiST (Girls in STEM at Tulane), I hosted a workshop that taught middle school girls about human osteology, bioarchaeology, and forensic anthropology. I made sure to tell the girls to ask questions, and share their ideas–there were no stupid questions and ideas in my lab. Whenever I asked a question (why do you think female pelves are different from male pelves? When do you remember when you got your first adult molar? ), the girls were not afraid to call out answers, nor were they afraid to answer my questions incorrectly. In fact, they loved sharing their ideas. In other words, they were brave, and did not care about giving the perfect answer. Hopefully this is a trend that continues.

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Ateles geoffroyi vellerosus Spider Monkey Central America mother and baby

Death without Weeping: Maternal Bonds towards Deceased Offspring among Non-Human Primates

Nonhuman primate mothers do not weep in response to death of their infants. When a non-human primate mother has her offspring, she has already invested considerably time as well as physical and metabolic energy to gestation and birth of the infant. Death of an infant, therefore, is detrimental to the mother who already invested in her offspring, as well as the group’s genetic continuity. Whether or not the death of non-human primate mother’s offspring elicits an emotional or affectionate response is more difficult to identify.

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Primatologists have long acknowledged the importance of death of a primate for calculations of demographic trends and constructing life tables (Altman and Altman, 1970). Studies of behavioral responses to death among rhesus macaques include elevated grooming levels between group members, possibly to counteract the loss of a group member. The living also engaged with the deceased by grooming, inspection, as well as aggression towards the corpse (Buhl et al., 2012). Female hamadryas baboons show increase in stress hormone levels after the death of a conspecific (Engh et al., 2006). Studies of chimpanzees group responses to pre- and post-death care of members of their cohort indicate that behaviors typically include close inspection and tests for signs of life at the moment of death, male aggression towards the corpse, all-night attendance by family members, cleaning of the corpse, and even avoidance of the place where death occurred (see Goodall, 1977, Anderson et al., 2010, and Biro et al., 2010).

Whether or not there exists a general trend of maternal responses to primate death remains poorly understood. The mother-offspring bond is considered to be one of the longest and most essential social bonds among mammals (Cronin et al., 2011). The maternal reposes associated with the permanent, premature disruption of this social bond—the death of the offspring—has rarely been investigated (Cronin et al., 2011). Early primatological studies documented male responses to dead infants among semi-free-ranging Barbary macaques (Merz, 1978). A long-term study of wild geladas from Ethiopia recorded 14 cases of dead infants being carried by females was the first attempt to explore responses to death in non-human primates, focusing on allomaternal-like behavior towards dead infant (Fashing et al., 2010). Primate death and behavioral responses from group members have also been documented from several sites, including the Gombe, Tai Forest, and safari park in Scotland (Teleki, 1973; Boesch and Boesch-Achermann, 2000; Anderson, 2011, respectively).

Primatological studies have documented instances when mothers continue to handle the corpses of their infants. Given this prolonged interaction, I wonder, does maternal attachment continues after the death of her offspring? If so, what triggers this particular behavior?

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Before I examine the behavioral responses to infant death, it is important to briefly describe what is considered “normal” mother-infant behavior among primate. Mothers and their infants represent a central focus of interest for other females in the group among species and groups of social primates (e.g. Hrdy 1976; Seyfarth 1976; Altmann 1980; Nicolson 1987; Maestripieri 1994a). Females visibly show their interest in interacting with newborn infants. When new infants are present in a group, subadult and nulliparous females approach the mothers and attempt to sniff, investigate, and pick up the young infants (Nicolson 1987). Females also have been observed grooming the mother in exchange for handling her new infant (Altmann, 1980, O’Brien & Robinson, 1991, Muroyama, 1994, Di Bitetti, 1997, Silk, 1999).

While female attraction to infants represents a common feature of primate species, maternal response to infant handling shows a certain degree of variability (Nicolson 1987; Maestripieri 1994b). Maternal responses to infant death have been attributed to several ecological and circumstantial explanations as well as several hypotheses in the primatological literature:

  • Unawareness of Death Hypothesis (Hrdy, 1999)
  • The Decomposition Hypothesis (Fashing et al., 2011)
  • Post-Parturient Condition Hypothesis (Kaplan, 1973; Biro et al., 2010)
  • “Learning to Mother” Hypothesis for Learning about Death (Warren and Williamson, 2004

Unawareness of Death Hypothesis

Extended carrying of a dead infant may indicate that the mother is unaware that her infant is no longer alive. According to the hypothesis, primate mothers of recently dead infants continue interacting with her infant exhibiting behaviors typical of new mothers, such as grooming and licking. For example, Kaplan (1972) recorded responses of captive female squirrel monkeys that were presented with the corpses of their dead infants. The infants had been dead for approximately two weeks. The mothers seemed unaware that their infant was no longer living, yet attempted to retrieve the corpse by lifting it or administer vocalizations regardless (Kaplan, 1972). However, these experiments do not simulate a situation that would occur in the squirrel monkeys’ natural environment. The mother’s infant was immediately retrieved after its death, which denied the mothers an opportunity to interact with her infant post-mortem.

Contrary to the hypothesis, there are examples of maternal behavior that shows the mother continues handling her infant while also exhibiting behaviors indicating that she is fully aware that her infant is no longer alive. A white-faced capuchin mother continued to groom and lick the body while trying to repel carnivorous insects from the corpse. She also allowed her dead infant to be fully submerged in water while she drank. Once she finished, she retrieved the corpse, and continued to transport her dead infant for several days (Perry and Manson, 2008). Similarly, chimpanzee mothers from Bossou, Guinea, appear to be aware that the bodies of the infants they carried were inanimate, and adopted carrying techniques not normally used with healthy juveniles (Biro et al., 2010).

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It is possible that uniparious mothers are unable to differentiation between living and non-living offspring due to a lack of experience. Studies have shown, however, that number of living offspring does not necessarily contribute to the duration for which in infant corpse is handled. Two multiparious snub-nosed monkey mothers carried and handled their dead infants for 4 days and one month. The mothers had had infants previously, and therefore could differentiate between normal, responsive infant behavior and abnormal, unresponsive infant behavior (Li et al., 2012). Similarly, multiparious chimpanzees mothers have been documented carrying their infant’s corpses for longer compared to the chimpanzee mothers carrying the corpse of their first and only offspring (Biro et al., 2010). Warren and Williamson (2004) also noted that two multiparious gorilla females also continued to handle their infants long after their death. Whether or not a primate mother is nulliparious or multiparious does not appear to influence how long she continues to interact with the corpse of her infant.

Overall, it appears that the unawareness of death hypothesis does not adequately explain the mechanism of maternal behaviors towards dead offspring. Continued handling of her infant does not necessarily suggest that she is unaware that her infant is not longer living; rather, the mother may be prolonging the separate from her infant for another reason.

The Decomposition Hypothesis

According to the decomposition hypothesis, any long-term carrying of the infant by the mother does not represent a sense of loss or attachment to the infant. Rather, mothers are unaware of the infant’s death and continue to carry the corpse until clear signals of decomposition (e.g. particular odor cues) indicate death (Fashing et al., 2010). Extreme climate conditions (such as cold or hot arid weather) slow the natural rate of decomposition of deceased bodies (Haglund and Sorg, 1997). Prolonged carrying (defined as longer than 10 days) of an infant corpse appears to be more likely in extreme climatic conditions, particularly in cold or hot arid weather, that naturally slows decomposition of infant body (Fashing et al., 2010).

Several studies of primates living in extreme climate conditions have supported the decomposition hypothesis. Gelada monkeys (Theropithecus gelada) of Guassa, Ethiopia, live in an extreme climatic condition that favors a slower rate of decomposition of dead individuals. Over a 3.75 year-long study period, 14 mothers carried and handled their mummified infants for 10 or more days. Extended carrying of dead infants has been documented among mountain gorillas that inhabit unusually cold environments (Fashing et al., 2010b, Nakagawa et al., 2010, Vedder, 1984) and chimpanzees living in extremely arid regions with a long dry season of Bossou, Guinea (Biro et al., 2010, Matsuzawa 1997).

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The decomposition hypothesis is based on another assumption that New World primates in tropical environments appear only to carry or care for dead infants rarely or for only a short period of time. For example, a tufted capuchin mother was reported to carry her dead infant for less than 24 hours after an infanticide attack (Izar et al., 2007). This behavior, however, may be due to the social dynamics of infanticide, rather than the maternal indifference towards her dead infant.

Despite the climatic circumstances that delay decomposition, primates have been documented to carry infants for a long enough period that the body does eventually decay. In this case, signs of decomposition, such as putrefaction and change in the infant’s appearance (e.g. loss of fur and limbs) do not repel mother and, in some cases, other kin and non-kin. For example, Bossou chimpanzee mothers as well as related and unrelated individuals from all age groups of both sexes attempted to handle, lift and drop limbs, and sniff the bodies of three dead infants. Juvenile and infants were even allowed to carry the bodies of infants some distance from the mother in bouts of play. Biro and colleagues (2010) state that they never observed a response that could be interpreted as aversion, despite the bodies’ intense smell of decay and usual appearance of mummified skin and missing fur.

Similarly, four female mountain gorilla continued to carry their dead offspring even when the corpses lost their hair and heads, and despite the pervasive smell of decaying flesh (Warren and Williamson, 2004). Observations made by Rumbaugh (1965) of captive squirrel monkeys in San Diego, California, noted that a mother continued to handle her infant for six weeks as the corpse began to putrefy. Over a 24-year study period of Japanese macaques, a total of 157 mothers continued to carry their dead infants between 1 to 17 days despite the quick progression of the decomposition, and the putrid smell and swarm of flies surrounding the dead infant and the mother (Sugiyama et al., 2009). In this case, however, non-kin avoided the mother and her dead infant, seemingly due to the smell, and she received less social grooming that before their infants had died (Sugiyame et al., 2009). Sugiyama and colleagues (2009) state that they cannot determine why mothers continue to carry the corpses given its bad state of decomposition. It is apparent, however, that mothers do not necessarily abandon their offspring due to aversion.

It is possible that “caretaking” behaviors rather than the environmental setting facilitates mummification. In the study conducted by Biro and colleagues (2010) in Bossou, Guinea, three chimpanzee mothers continued to carry the mummified corpses of their infants for 19, 27, and 68 days following their death, exhibiting extensive care of the body by grooming it regularly, sharing her day and night nests with it, and showing distress whenever they became separated. The mothers also chased away flies that circled the corpses, twice with the aid of a tool (Biro et al., 2010).

In sum, the decomposition hypothesis has several flaws. Infant handling is not limited to primates living in unusually arid, cold regions. In fact, mothers continue to handle their dead infants even though the corpses admit olfactory and visual signs of putrefaction and decomposition. Overall, it seems that the foul odor of decomposing flesh does not appear to deter mothers from transporting and manipulating corpses. Oftentimes, this “care-taking” behavior seems to (unintentionally?) preserve the offspring. Yet, this treatment towards dead infants will be explored in the post-parturient condition hypothesis.

Post-Parturient Condition Hypothesis

Post-parturient condition hypothesis proposes that postpartum hormones influence maternal behaviors toward dead infants. Physical characteristics and particular hormones are essential for the onset and maintenance of infant-carrying behavior and the development of the mother–infant bond towards living infants (Kaplan 1973; Biro et al. 2010). Neuroendocrine mechanisms and physical characteristics of the infant (such as natal attractiveness) stimulate and regulate motherly behavior to care for and protect her offspring (see Maestripieri, 2001, 1991). At birth, an infant’s attractiveness includes size at birth, vocalizations made by the infant (e.g. “purring” noises), infantile facial expressions, distinguishing morphological features such as bug ears or tail tufts, and distinctive coat color (Hrdy, 1976).

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Human, non-human primate, and non-primate mammal studies demonstrate that there are endocrine influences on mother-infant interactions and the formation of bond post-partum (Maestripieri, 1999). In non-primate mammals, pregnancy and lactation hormones enhance maternal responsiveness and behavior although they are not strictly necessary for their onset or maintenance (Stern, 1989). In New World monkeys such as red-bellied tamarins (Saguinus labiatus) and common marmosets (Callithrix jacchus), there is evidence that hormones influence both responsiveness to young during pregnancy and quality of maternal care during lactation (Pryce et al., 1993). Studies of group-living pigtail macaque females show that the females increased their rate of interaction with infants during the final weeks of pregnancy that corresponded with an increase in plasma levels of estradiol and progesterone (Maestripieri and Wallen, 1995; Maestripieri and Zehr, 1998). Fleming and colleagues (1997) showed that human mothers who maintained high levels of estradiol over the parturitional period also had higher feelings of attachment to their own infant in the early postpartum days than mothers whose estradiol levels dropped. Thus, these studies indicate that primate and human parenting is partially influenced by physiological variables.

The continued interaction and gradual separation between the mother and infants’ bodies appears to also be a by-product of hormonal condition of pregnancy and the formation of the mother-infant bond in post-parturient female primates. Behavioral studies note that mothers do not simply abandon the corpse of her dead infant. Rather, the mother continues to interact with the corpse, gradually separate herself physically from the body of her dead offspring.

There are several physiological characteristics that may be observed in female primates that indicate that hormone levels are fluctuating and therefore influencing her behavior. Postpartum amenorrhea in chimpanzees lasts around four years, but is shortened with the death of an infant (Wallis, 1997). The infant could no longer breastfeed and lactation ceased, triggering the mothers’ reproductive cycle to return.

To date, there are no studies that directly link changes in hormones during the mother’s transition from handling her infant until the moment she abandons its. Therefore, the post-parturient condition hypothesis relies on behavioral studies. Several behavioral studies report that mothers gradually separate herself from the corpse of her infant. For example, gelada monkey mothers also experience a graduate separation that includes a transition from only the mother handling the infant corpse, and then allowing other group members to handle to deceased juvenile (Fashing et al., 2010).

The post-parturient condition is best illustrated by observations conducted at Chimfunshi Wildlife Orphanage Trust, a chimpanzee sanctuary in Northwest Zambia (Cronin et al., 2010). Shortly after the death of her infant, the mother transitioned from maintaining close, constant proximity to the dead body to creating physical distance from the deceased infant (Cronin et al., 2010). She maintained visual contact with the body when not in immediate proximity to it. As time passes, mothers transition to lessening her contact with the body and allowing others to inspect the body (Biro et al., 2010; Hosaka et al., 2000). Other studies have also reported that chimpanzee mothers gradually transition from extreme attachment to the body of their dead infants immediately following death to weakened attachment to the body as time passes (Hosaka et al., 2000, Biro et al., 2010).

Ring-talked lemur (Lemu catta) mothers have been reported to continue to return to their dead infants several times for several hours after the infant’s death. Every time each female returned to the body, she would sniff, lick, and touch the infant (Nakamichi et al., 1996). Despite the increasing distance between the troop and the deceased infant, the mothers continued to return to her dead infant, even when the troop have moved 400 meters away from the corpse (Nakamichi et al., 1996). Six of the seven mothers attempted to lift the corpses, and one mother clumsily carried the corpse 15 meters and attempted to jump into a tree. Mothers were unable to maintain proximity between both the troop and the corpse concurrently because she was not able to carry her dead offspring (Nakamichi et al., 1996).

The post-parturient hypothesis appears to most adequately examine the mechanism of maternal handling and carrying of deceased infant remains. Carrying and handling a corpse after death expresses a strong attachment, and the gradual separation of mother from her dead infant are behavioral responses to hormonal changes. Whether or not death of an infant elicits a psychological or emotion response is difficult, possibly impossible to identify. To compliment the hormonal-centric tenants of the post-parturient hypothesis, I will explore literature that contemplates whether or not the prolonged carrying and handling of corpses is part of process in which primates “learn” about death.

“Learning to Mother” Hypothesis for Learning about Death

Studies of maternal responses to death among apes provide additional information investigating whether or not the extended interaction with infant corpses is a period during which primates engage in a learning process. The “learning to mother” hypothesis was first proposed by Hrdy (1976) to explain why female young and non-mothers interact so frequently with offspring. Warren and Williamson (2004) adapt this hypothesis to a population of mountain gorillas to illustrate that the prolonged handling of dead infants is a type of social learning for mothers, young, and non-mothers to acquaint themselves with cues typical of death.

Ateles geoffroyi vellerosus Spider Monkey Central America mother and baby

Primatologists have investigated the long-term benefits of young and non-mothers carrying living infants. The handling of live infants by non- mothers has been referred to as aunting, baby-sitting, kidnapping, play-mothering, allomaternal behavior, or allomothering (Hrdy, 1976; Maestripieri, 1994a, 1994b). According to the ‘‘learning to mother’’ hypothesis, young or nulliparous females who handle infants gain maternal experience, and recalling these skills later in life, making them more capable of raising their own offspring (Hrdy, 1976).

The benefits of “learning to mother,” could be gained with a corpse, since the motor skills required to carry an infant while traveling and foraging could still be acquired (Warren and Williamson, 2004). Furthermore, the extending carrying behavior by the mothers, as well as related and unrelated individuals, may be an example of observational learning that promotes prolonged transport of deceased young (Biro et al., 2010). These interactions with a corpse could be part of a process in which the primate learns to recognize death.

Observations of mountain gorillas at Karisoke Research Center, Rwanda, noted that two nullparious mothers in their final months of pregnancy, and two mothers who had recently lost offspring all handled and transported the mothers’ two dead infants (Warren and Williamson, 2004). As previously discussed, the hormonal disposition of the mother may contribute to the continued handle of her infant after death. The hormonal state of pregnant females similarly predisposes her to interact more frequently with infants, even ones that are recently dead. It seems it may be both an innate change in her physiology as well as an opportunity to practice handling infants.

Similarly, Cronin and colleagues (2010) suggest that chimpanzees handle and examine the body of deceased infants in order to recognize cues of a corpse and therefore “learn” about death. Studies conducted at Chimfunshi Wildlife Orphanage Trust, a chimpanzee sanctuary in Northwest Zambia, recorded that one chimpanzee mother touched the body and face of her dead infant, presumably an action that would have provided olfactory and gustatory information about the infant’s condition (Cronin et al., 2010). Every time she returned to the infant’s corpse, she would closely inspected its face and neck. Cronin and colleagues (2010) suggest that close inspection of the face could serve as the best location to assess the condition of the infant. No changes in eye gaze, breathing, or facial musculature could inform the mother that the infant’s condition had irreversible changed (Cronin et al., 2010). The mother was actively gathering novel sensory information about the dead infant, possibly remembering this information for the next time she encountered the same set of cues. In other words, the mother may have been “learning about death.” (Cronin et al., 2010: 420).

Whether or not prolonged handling of infants is indicative of a “cultural” behavior towards death that is passed on throughout the group and through generations may be impossible to prove. Yet, some researchers suggest that the transmission of knowledge for handling of dead infants that occurs throughout multiple generations and occurs among multiple members of a group may indicate that this learning and knowledge may be transferred (see Cronin et al., 2010; Warren and Williamson, 2004; and Biro et al., 2010). For example, three chimpanzee mothers at Bossou, Guinea, all had infants that died during the study period and all exhibited a similar manner of prolonged handling of dead infants. Biro and colleagues (2010) suggest that the similarities in treatments and behaviors may not be a rare occurrence in this particular community. In fact, the prolonged handling may part of the culture of that particular group. In sum, the learning to mother hypothesis provides an intriguing framework in which primatologists may explore prolonged infant handling among the great apes.

Mother-Infant Bonds and Learning to Grieve?

Overall, it appears there is continued attraction and care towards dead infants occurs to some extent in all major taxaonomic groups (Anderson, 2011). Both the decomposition and unawareness of death hypotheses seem insufficient to explain why primate mothers continue to handle the corpses of offspring after death. Contrary to the unawareness of death hypothesis, primate mothers appear to handle their infants in ways that suggest they are aware that their offspring is no longer living. Similarly, primate mothers continue to handle their dead infants regardless of the environmental setting (arid verses humid) and despite putrefaction and decomposition of the corpse.

The post-parturient condition hypothesis, on the other hand, considers both the behavioral and hormonal responses of primate mothers across primate taxa. The formation of the strong mother-infant bond at birth does not simply disappear once the infant dies; rather, it seems that the mother transitions from physiological conditions typical of motherhood (e.g. cessation of lactation amenorrhea) is concurrent with the mother’s gradual separation from and abandonment of her deceased infant.

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It is particularly interesting that mothers slowly allow conspecifics to handle the corpse, and that recognition of particular cues that signal death may illustrate that young and non-mothers are “learning” to recognize death. Whether or not the handling of dead infants should be considered cultural learning is difficult and potentially impossible to identify. Given that multiple mothers of a particular group of chimpanzees and gorillas all exhibited similar behaviors in response to the death of their infant indicates that the behavior may be contributed to both physiological and social influences.

Studies of primate death are greatly biased towards chimpanzees, but long-term and behavioral studies of gorillas, baboons, and new world monkeys are also becoming more common. Overall, primate behavioral and hormonal studies indicate that continued handling and interaction with infant corpses signifies a connection between the mother and her offspring, even if the offspring has died.

Bibliography

Altmann, J. 1980. Baboon Mothers and Infants. Cambridge, MA: Harvard University Press.

 

Altmann SA, Altmann J. 1970. Baboon ecology: African field research. Chicago: University of Chicago Press.

 

Anderson, JR. 2011. A Primatological Perspective on Death. American Journal of Primatology Commentary 73: 410-414.

 

Biro D, Humle T, Koops K, Sousa C, Hayashi M, Matsuzawa T. 2010. Chimpanzee mothers at Bossou, Guinea carry the mummified remains of their dead infants. Current Biology 20:R351–R352.

 

Boesch C, Boesch-Achermann H. 2000. The chimpanzees of the Ta ̈ı Forest: behavioural ecology and evolution. Oxford: Oxford University Press.

 

Buhl, JS, Aure, B, Ruiz-Lambides, A, Gonzales-Martinez, J, Platt, ML, Brent, LJN. 2012. Reponses of Rhesus Macaques (Macaca mulatta) to the Body of a Group Member That Died from a Fatal Attack. International Journal of Primatology 22: 860-871.

 

Cronin, KA, Van Leeuwen, EJC, Mulgenga, IC, Bodamer, MD. 2010. Behavioral Responses of a Chimpanzee Mother Toward her Death Infant. American Journal of Primatology 73: 415-421.

 

Di Bitetti, MS. 1997. Evidence for an important social role of allogrooming in a playtrrhine primate. Animal Behaviour 54: 199-211.

 

Engh, AL, Beehner, JC, Bergman, TJ, Whitten, PL, Hoffmeier, RR, Seyfarth, RM. 2006. Behavioral and hormonal responses to predation in female chacma baboons (Papio hamadryas ursinus). Proceedings of the Royal Society of London B: Biological Sciences 272: 707-712.

 

Fashing P, Nguyen N, Barry T, Goodale C, Burke R, Jones S, Kerby J, Lee L, Nurmi N, Venkataraman V. 2010a. Death among geladas (Theropithecus gelada): a broader perspective on mummified infants and primate thanatology. American Journal of Primatology 71:1–5.
Fashing P, Nguyen, N, Fashing NJ. 2010b. Behavior of geladas and other endemic wildlife during a desert locust outbreak at Guassa, Ethiopia: ecological and conservation implications. Primates 51: 193-197.

 

Fleming, AS, Ruble, D, Krieger, H, Wong, PY. 1997. Hormonal and experiential correlates of maternal responsiveness during pregnancy and the puerperium in human mothers. Hormones and Behavior 31: 145-158.

 

Goodall, 1977. 1977. Killings and Cannibalism in Free-Living Chimpanzees. Folia Primatologica 28: 259-282.

 

Haglund, WD, Sorg MH, editors. 1997. Forensic taphonomy: the postmortem fate of human remains. Boca Raton: CRC Press.

 

Hamai, M, Nishida, T., Takasaki, H, Turner, LA. 1992. New Records of Within-group Infanticide and Cannibalism in Wild Chimpanzees. Primates 33(2) 151-162.

Hosaka, K, Matsumoto-Oda, A, Huffman, MA, Kawanaka, K. 2000. Reactions to dead bodies of conspecifics by wild chimpanzees in the Mahale Mountains, Tanzania. Primate Research 16: 1-15.

 

Hrdy, SB. 1999. Mother nature: a history of mothers, infants, and natural selection. Pantheon Books, New York.

 

Hrdy, SB. 1976. Care and exploitation of nonhuman primate infants by conspecifics other than the mother. In: Advances in the study of behavior vol 6. (Ed. by Rosenblatt JS, Hinde RA, E S, Bier C) New York: Academic Press. 101–158

 

Izar, P. Ramos da Silva, ED, De Resende, BD. Ottoni, EB. 2007. A case of infanticide in tufted capuchin monkeys (Cebus nigritus). Mastozoologîa neotropical 14(1) 73-76.

 

Kaplan, J. 1973. Responses of mother squirrel monkeys to death infants. Primates 14: 89-91.

 

Li, T, Ren, B, Li, D, Shang, Y, Li, M. 2012. Maternal responses to dead infants in Yunnan snub-nosed monkey (Rhinopithecus bieti) in the Baimaxueschan Nature Reserve, Yunnan, China. Primates 52: 127-132.

 

Maestripieri, D. 2001. Is There Mother-Infant Bonding in Primates? Developmental Review 21: 93-120.

 

Maestripieri, D. 1999. The biological of human parenting: insights from nonhuman primates. Neruoscience and Biobehavioral Review 23: 411-422.

 

Maestripieri, D. 1994a. Mother-infant relationships in three species of macaques (Macaca mulatta, M. nemestrina, M. arctodies). I. Development of the mother-infant relationship in the first three months. Behaviour 131: 75-96.

 

Maestripieri, D. 1994b. Social structure, infant handling, and mothering styles in group-living Old World monkeys. International Journal of Primatology 15: 531-553.

 

Maestripieri, D, Wallen, K. 1995. Interest in infants varies with reproductive condition in group-living female pigtail macaques (Macaca nemestrina). Physiological Behavior 57: 353-358.

 

Maestripieri, D, Zehr, JL. 1998. Maternal responsiveness increases during pregnancy and after estrogen treatment in macaques. Hormones and Behavior 34(3): 223-230.

 

Matsuzawa, T. 1997. The death of an infant chimpanzee at Bossou, Guinea. Pan African News 4:1.

 

Merz, E. 1978. Male-male interactions with dead infants in Macaca sylvanus. Primates 19: 749-754.

 

Muroyama, Y. 1994. Exchange of grooming for allomothering in female patas monkeys. Behaviour 128: 103-119.

 

Nakagawa N, Nakamichi M, Sugiura, H, editors. 2010. The Japanese macaques. New York: Springer.

 

Nakamichi M, Koyama N, Jolly A. 1996. Maternal responses to dead and dying infants in wild troops of ring-tailed lemurs at the Berenty Reserve, Madagascar. International Journal of Primatology 17:505–523.

 

Nicolson, NA. 1987. Infants, mothers, and other females. In: Primate Societies (Ed. by B. Smuts, D. Cheney, R. Seyfarth, R. Wrangham & T. Struhsaker) 330-342. Chicago: Chicago University Press.

 

O’Brien, TG and Robinson, JC. 1991. Allomaternal care by female wedge-capped capuchin monkeys: effects of age, rank and relatedness. Behaviour 119: 30-50.

 

Perry S, Manson JH. 2008. Manipulative monkeys: the capuchins of Lomas Barbudal. Cambridge, MA: Harvard University Press.

 

Pryce, CR, Dobeli, M, Martin, RD, 1993. Effects of sex steroids on maternal motivation in the common marmoset (Callithrix jacchus), development and application of an operant system with maternal reinforcement. Journal of Comparative Psychology 107: 99-115.

 

Rosenson, LM. 1977. The response of some prosimian primate mothers to their own anesthetized infants. Primates 18: 579-588

 

Rumbaugh DM. 1965. Maternal care in relation to infant behavior in the squirrel monkey. Psychological Reports 16: 171–176.

 

Scheper-Hughes, N. 1992. Death Without Weeping: The Violence of Everyday Life in Brazil. Berkeley, CA: University of California Press.

 

Scheper-Hughes, N. 1984. Infant mortality and infant care: Cultural and economic constraints on nurturing in Northeast Brazil. Social Science & Medicine 19(5): 535-546.

 

Seyfarth, RM. 1976. Social relationships among adult female baboons. Animal Behavior 24: 917–938

 

Silk, JB. 1999. Why are infants so attractive to others? The form and function of infant handling in bonnet macaques. Animal Behaviour 57: 1021-1032.

 

Stern, J. 1989. Maternal Behavior: Sensory, Hormonal, and Neural Determinants. In: Psychoendocrinology (Ed. by FR Brush, S Levine) 105-225 San Diego, CA: Academic Press.

 

Sugiyama, Y, Kurita, H, Matsui, T, Kimoto, S, Shimomura, T. 2009. Carrying of dead infants by Japanese macaques (Macaca fuscata) mothers. Anthropological Science 117: 113-119.

 

Teleki G. 1973. Group responses to the accidental death of a chimpanzee in Gombe National Park, Tanzania. Folia Primatologica 20:81–94.

 

Vedder, A. 1984. Movements patterns of a group of free-ranging mountain gorillas (Gorilla gorilla beringei) and their relation to food availability. American Journal of Primatology 7: 73-88.

 

Wallis, J. 1997. A survey of reproductive parameters in the free-ranging chimpanzees of Gombe National Park. J. Reprod. Fertil. 109: 297–307.

 

Warren Y, Williamson EA. 2004. Transport of dead infant mountain gorillas by mothers and unrelated females. Zoo Biology 23:375–378.

 

 

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Mummies, Saints, and Religion in the Andes

Andean peoples have a long history of incorporating new practices into their worldview. Just as the Inka institutionalized ritual life during the Late Intermediate Period (1000-1450 AD), Andean people were able to incorporate the rituals of Catholicism into their own religious framework after the Spanish conquest. In Catholicism, the body—be it the body of a deceased Christian, a saint, or the body of Christ—was used to convey meanings about life, death, and the promise of an ideal afterlife in exchange for devout living. Similarly, the body had an equally ritualistic role among the Andean people as ancestral mummies were consulted on matters of life and venerated long after death. In other words, the body in its preserved, mummified form had similar roles in Catholicism and Andean religion. The he fusing together two separate ideologies (Andean beliefs and Catholicism), or syncretism, may have been partly due to the importance the Andean people placed on mummified bodies. What are the similar ways  Andean people and Catholics from Europe perceived the body?

The body is not simply a biological entity, but is a carefully crafted artifact that continues to be worked and transformed after death. In death, the body transforms into a form of material culture created and maintained through social practices, historical circumstances, and other social forces (Sofaer, 2006). The body is used to convey representations of death and the afterlife, of a society´s boundaries, of the nature of humanness, and of the ordering of the social world. The treatment of the corpse embodies complex concepts about the living body (what it is to be human, how to follow codes of conduct) and society at large (how the social order is represented but also about the nature of death) (Pearson, 2008).

The dead, mummies in particular, were seen as an active group in the Andean world. One of the best-known techniques of transforming and utilizing the corpse is by means of its transformation into a mummy. Such bodies retained what Tung (2014) refers to as “post-mortem agency” in which the bodies, even in their altered, mummified state, remain politically and social active in death. These bodies are the culmination of rituals that serve to separate the dead from the living and install them within another dimension of human understanding (Pearson, 2008). Interestingly, the perceptions of the mummified body were similar between Catholics and Andean people, and, as I argue, allowed for the syncretism of Catholicism and Andean religion.

Mummification and Ancestor Veneration in Andean Religion

The Andean peoples had long venerated their ancestors and the mummified the remains of their most important relatives (mallquis), but the Inka institutionalized this process of ancestor worship by creating a system of religious corporations (panacas) to honor deceased rulers (Andrian, 2001). Theses practices continued through the Inka period and desiccation of the body continued to be the most notable funerary practice throughout the Andes at Spanish contact (Rakita and Buikstra, 2005).

After death, the living exerted great effort to embalm the body of the Inka emperor in a manner that preserved his appearance and likeness as in life (Cobo, 1990 [1653]; Cieza de León (1959 [1553]). The mummified Inka emperors were wrapped in large amounts of cotton and dressed in rich clothing and were enshrined in golden thrones in the Temple del Sol (Korikancha) in Cusco (Dillehay, 1991), or in their own homes where kin could provide attention and care for their bodies (Rowe, 1995). Cobo (1653, 1990) notes that some bodies over 200 years old were still found in Cusco and were so well preserved that the skin and hair were still intact, as if the individual had died less than a month before!

A portion of the gold and silver the deceased had accumulated in his lifetime were placed with the body while other sumptuary goods were buried elsewhere, specifically in places where the deceased usually went to enjoy himself during his life (Cobo, 1990 [1653]). A separate set of priests made offerings to the mummies of deceased Inkas and other prominent figures, providing ritual meals of chicha and other foodstuff, surrounding them with utensils used in life (such as textiles, hoes, and weapons), and including them to community religious celebrations (Cobo, 1990 [1653]); Cieza de León, 1959 [1553]).

From Felipe Guaman Poma de Ayala: El primer nueva corónica y buen gobierno

The body of the dead Inka emperor was dried and preserved above ground, guarded by attendants, and treated as if the ruler were still alive (Dillehay, 1995). The body itself preserved the memory of the dead ruler, and his descendants recited his deeds on public occasions. The mummified Inka rulers participated in public affairs, were brought to temples and houses to carry out functions that, in all appearances, were of a political character. For example, they were regularly borne on litters during the most important ceremonies that took place in Cusco’s plaza and often consulted on important matters (Pizarro, 1978 [1571]).

The palaces and other residences of a deceased ruler were not inherited by his successors; rather, the dead physically and symbolically were still believed to occupy their residences and palaces even in death. These residences served as monumental reminders of the ruler (Rowe, 1995). In other words, the deceased Inka ruler continued to physically and symbolically participate in society; he did not and could not wholly die.

Are there any similarities between the bodies of the Inka and Catholic bodies?

Incorruptible Catholic Bodies

The Roman Catholic Church has long practiced mummification to preserve the bodies of saints, priests, bishops, and other high-ranking church members. The bodies are named “incorruptible” because the bodies are believed to have preserved miraculously and are immune to decay (Jeremiah, 2012; Chamberlain and Pearson, 2001). The spontaneous preservation was believed to be evidence of the sanctity of the individual (Jeremiah, 2012; Chamberlain and Pearson, 2001); an individual believed to be pure and lived what is considered an “uncorrupted” life. While many of the so-called incorruptible bodies have been deemed as forgeries, the perception of the incorruptible nature of the bodies continues in the Catholic mindset (Jeremiah, 2012).

The display of these incorruptible bodies belonging to saints, priests, bishops, and other high-ranking individuals in the Catholic Church serves several purposes. Displaying bodies of the deceased functions as a constant reminder of the inevitability of death to encourage followers of the Catholic faith to live devout lives. Also, bodies belonging to divine individuals are believed to be immediate sources of supernatural power for good or for ill, and close contact with them or possession of them was a means of participating in that power (Geary, 1986: 176). Beginning in the 11th century and into the present, whole and partial bodies of saints were prized for their thaumaturgic power, particularly “their ability to substitute for public authority, protest and secure the community, determine the relative status of individuals and churches, and provide for the community´s economic prosperity” (Geary, 1986: 179). In sum, mummified bodies served religious as well as social, economic, and political purposes ultimately to legitimate the authority of the Roman Catholic Church.

Mummied head believed to belong to St. Catherine of Siena, Basilica Cateriniana San Domenico, Siena, Italy

Spanish Conquest and Dismantlement of Ancestor Veneration

The Spanish justified their conquest of Tawantinsuyu in 1532 by vowing to convert the indigenous souls with their pagan beliefs to the Catholic faith (Andrien, 2008). While the conquistadors initially sought the treasure held by mummy and their shrines, Spaniards quickly realized that the mummies were dangerous because they commanded considerable political and religious authority; they were still conferred with, and capable of, inspiring their followers to action against Spanish rule (Dean, 2010). Spaniards rapidly recognized the danger posed by the cadavers of the divine, ancestral deceased, control over the dead—both the bodies of the deceased and beliefs about them—was a critical element in the conversion efforts of early Christian evangelizers in the Andes (Harris, 1982).

Body, Soul, and the Afterlife: Modern Ethnographic Examples 

The idea that the spiritual identity and power of the dead is located in their desiccated physical remains is a very old one in the Andes. According to Inka religious traditions, the dead would reach their final destination or resting place (pacarina) after the performance of specific rituals and mummification. Yet, the individual’s mummified corpse and the objects belonging to that individual during life are both believed to house the essence of the individual after death while the essence of the individual journeyed to the afterlife simultaneously (Andrien, 2008; Dillehay, 1995). Similarly, in Catholicism, the deceased also go through a transition into the afterlife (heaven), while both the body and the objects associated with the individual continues to be sacred and possess the essence of the individual (Jeremiah, 2012).

In modern-day Peru, indigenous people in Huaquirca, Department Apurímac, Peru, prepare and process in a complex ritual of combining aspects of both Catholicism and Andean beliefs to ensure the soul reaches the afterlife. While a portion of Huaquircaños physically burry the deceased in a Christian burial, others preform a clothes-washing ceremony of the deceased’s clothing. This clothes-washing ceremony ensures that the soul does not return to the clothing he or she wore during life, but instead continues onto the afterlife (Gose, 1994). Similar to the Inka mummies, objects and the places the Huaquircaños habited during life potentially continue to possess the soul of the deceased (Gose, 1994).

The Sonqueños of the south-central highlands of Peru combine their indigenous Andean beliefs with Christian ideas about the afterlife. The Sonqueños burry their dead in their cemetery in the Christian tradition, yet they conceptually locate their ancestors in the chullpas (burial houses or towers) on their sacred hill located near their village (Allen, 2002). While the bodies are physically the cemetery and conceptually occupy the chullpas, the souls, or essences, of the deceased also travel to what the Sonqueños refer to as hanan pacha (upper world), which they also define as the Christian heaven (Allen, 2002). Thus, the concepts of the afterlife do not diverge dramatically from the original Andean beliefs; rather, the concepts of the afterlife are incorporated into the Catholic worldview.

Purity of the Preserved Body

Inka mummies were ancestors that were meant to be visited and preform as oracles. It would therefore follow that the preservation of their corporeal form was imperative. In fact, during the Spanish extirpation, Andean people removed the bodies because the deceased from Catholic cemeteries. They reported that the dead were unhappy with burial; they were alone and isolated, unable to breathe and move under the weight of the earth, and overwhelmed by the stench of their own rotting flesh which had not been allowed to desiccate naturally in the cool, arid air of the traditional crypt-cave (Doyle, 1988). Among the modern-day Sonqueños in Peru, Allen (2002) notes that after death, a sinful individual is unable to accomplish his or her transformation from the body to the afterlife, and therefore be forced to animate its rotting body.

Similarly, Catholic bodies of iconic religion figures preserved due to the purity of soul; they are thus the ideal examples of upholders of the Catholic faith (Jeremiah, 2012). The body of Margaret of Cortona (1247-1297), for example, did not decay after her death, but instead gave off a pleasant sent that was interpreted as the Odor of Sanctity. Her remarkable preservation later led to her canonization (Vago, 2007) and status as an incorruptible body in the Catholic Church (Jeremiah, 2012). The bodies of the ideal Catholic, therefore, would be spiritually pure and therefore immune to decay or putrefaction.

St. Margaret of Cortona

The importance of purity and perfection in the Inka ideology is best illustrated in the qhapaq huchas, or capacocha, a ceremony during which female and male children and teenagers of exemplary of physical purity and perfection, known as ahapaq hucha, were immolate tributes to the Inka Empire (Besom, 2010). Typically, the qhapaq huchas were virgin boys, girls, and young women who were selected specifically for their good looks and lack of blemishes such as warts, freckles (Cobo 1979: 235-238 [1653]; 1990: 111-113 [1653]).

The capacocha involved leaving objects in a burial that in some way mirrored, either literally or metaphorically, the deceased (Gaither et al., 2008: 108, 113, 115-116). The ahapaq hucha would be enshrined with objects that denote markers of gender and, arguably, objects representing the ideal professions and behaviors of living males and females. For example, feminine statuettes and markers of gender, such as tipus, were deposited with girls and young women (Ceruti, 2003; Linares, 1966; Reinhard 1996, 1999; Reinhard and Ceruti, 2000). Females and female statuettes were dressed like aqlla-kuna “chosen women,” who were virgins who served as imperial gods of state (Besom 2009). Camelids were exclusively placed with boys, perhaps because in Andean society it is usually males who herd and are in charge of the llama caravans (Besom, 2009).

In sum, both Catholicism and Andean religion place emphasis on the sacredness of unblemished bodies as an indication of the purity of the individual. The bodies of the saints were physical representations of the ideal Catholic. The ahapaq huchas, similarly, were meant to embody the ideas of perfection, both physically as well as in their gendered professions.

Inka Burial Objects and Catholic Relics

Statues depicting divine individuals are used as objects of veneration and meditation in religions worldwide. The Catholic Church defines relics as the remains of a saint or holy person. There are three tiers of relics: 1) saints’ bodies and instruments involved in the crucifixion of Christ, 2) objects in close contact with a saint, such as clothing or instruments of martyrdom, and 3) objects touched by a saint (Edwards, 1997). Jewel-encrusted reliquaries to hold the relics, images of the saints and other holy persons also had considerable religion value and power in the Roman Catholic church and were therefore installed securely in the chancels of the richest monasteries and cathedrals of Europe (Jeremiah, 2012).

The physical body of the saint, however, maintains the most power in the Roman Catholic faith. The bodies, and sometimes body parts, of a specific saint were thought to possess the spiritual essence of the deceased. These saints were believed to be simultaneously present in the bodily remains and in heave also (Bynum, 1995). When a saint or high-ranking member of the church died, the body is preserved and the pieces of the body, or even pieces of clothing or objects that belong to the individual are sent to various locations (Jeremiah, 2012).

Possession of a relic body, piece of the body, and/or object belonging to the deceased was beneficial because the church or temple that houses these objects would become an important site for pilgrimages, and therefore made more money (Sharf, 1992). These bodies and body parts were believed to be reservoirs of divine energy with the power to protection and even offer advice and guidance to the faithful (Jeremiah, 2012).

Saint Coronatus, Heiligkreuztal, Germany

Similarly, the Andean people and the Inka shared similar viewpoints on the sacred nature of the body as well as the objects formally belonging to the deceased. Some of the of the treasures belonging to the deceased Inka were enshrined with the mummy, yet many objects were buried or placed in places where the deceased occupied during life (Cobo, 1990 [1653]). Because these objects were made for the ruler’s use when he was alive, Inka believed that no other person should use these objects after his death; they were considered property and remain at the service of their owner (Cobo, 1990 [1653]).

A variety of artifacts that denote the individual’s sacred status would accompany the qhapaq hucha during the capacocha. A male qhapaq hucha would be carefully entombed in a pit or bottom of a deep shaft. He would be seated, and around him would be placed or he would wear various offerings—Spondylus shell, an llawt´u (head band), a medallion, and a bracelet (Besom, 2009), along with anthropomorphic and zoomorphic statuettes made from gold, silver, copper, or Spondylus (Besom, 2010).

Just as relics served to connect Catholic cathedrals along pilgrimage routes oriented around Vatican City—the seat of the Roman Catholic faith, the qhapaq hucha were immolated in shrines that had a particular relationship with the Inka capital, Cusco. Cusco was the center of the ceque system—a series of imagined, ritual pathways radiating from Cusco and along which sacred shrines, or huacas, were placed (Bauer, 1992). Bernabé Cobo (1990 [1563]) first noted that the ceques of Cusco radiated out from the Koricancha and Bauer (1992) later found that many ceques do in fact originate at the Inka’s main temple.

Interestingly, the ceques, shrines, and the capacocha ceremony all may be intertwined. During capacocha, the selected children were taken to Cuzco and then distributed to the principal huacas—places believed to be imbued with sacred power—to be ritually sacrificed. These places were sacred shrines and sites in and around Cusco that were specifically for the offerings of children. Shrines that were further away required long processions and upon their arrival took part in festivals (Besom, 2010). Additionally, a number of Inka shrines had an oracular function, so whenever the Inkas asked for advice on important matters, they dispatched children to these shrines as immolations (Besom, 2010).

Besom (2009) argues that the child sacrifices reified the social stricter and political organization of the empire, particularly the asymmetrical relationship between Cuzco, the center of political and religious authority in the state, and the hinterlands. The capacocha was also intertwined with Inka economy—preforming these ceremonies were vital to good weather, water availability, and agricultural production (Benson, 2009). Considering the socio-economic and religious importance of the shrines and the qhapaq hucha, the capacocha ceremony is a religion procession that resembles a pilgrimage. Shrines are similar to churches and holy places that enshrine relics and the qhapaq hucha are, indeed, similar to the relics themselves. Interestingly, the ceque system links many of the shrines to Cusco as well as the Inka’s main temple—the Koriconcha—while Catholic churches also conceptually link themselves to the center of the Roman Catholic Church—the Vatican.

Capacocha of teenage girl, Museum of High Altitude Archaeology, Salta, Argentina

Bodies of Ancestors and Saints

The Catholic incursion into Peru sought to displace the visible role of the dead in the construction of social organization within the community (Sillar, 1992). In particular, the Spanish imposed a series of saint day celebrations; yet, such saint days have been adapted to serve the needs of Andean communities (Sillar, 1992). New Spanish towns in the Andes were named for a saint, and the likenesses of martyrs, apostles, and founders of religious orders were placed alongside images of Christ and the Virgin in the altar decorations and murals of churches. In the Andes, the annual celebration of the town’s patron became a major event in public ritual life. Individual saints were remembered on a daily basis. In fact, Felipe Guaman Poma, an Andean chronicler, incorporated the feasts of the saints in his monthly calendar of colonial Andean ceremonial life (Guaman Poma de Ayala, 1980 [1615/1616]).

Despite these incorporations of saints and celebrations into Andean life, indigenous populations continued to treat images and statues of saints in the same manner they treated their ancestral mummies. Chroniclers wrote that the Andean people intentionally mummified the bodies of their forbearers in order to worship them. The spirit of the ancestral mummy was thought to reside in the group’s place of origin, and could be called back to the mummy for consultation (Salomon, 1995). Jesuit missionary Jose de Acosta argued that the transformation of a body, in this case the body of an Andean ancestor, into an object of veneration was the equivalent to making what the Spanish missionaries deemed a “false” religious image, or idol. (Ramos, 2010).

All Saints’ Day, Peru

A religion that combines Catholic as well as Andean perceptions on the nature of ancestral and saints’ bodies persists in modern-day Peru. The ceremony of Corpus Cristi preformed by the Sonqueños in south-central Peru is an excellent example that demonstrates the syncretism between Inka capacocha ceremony and Catholic religious celebrations. Corpus Cristi is a moveable feast, falling in late May or June (on Thursday after Trinity Sunday). About thirty Sonqueños embark on an arduous journey to the distant peaks of Qoyllur Riti range. According to legend, a miracle took place at Qoyllur Riti: the Christ Child appeared to a shepherd boy from the nearby village of Tayankani. After playing with the shepherd boy, the Christ Child disappeared into a rock, which was ever after marked with his imprint (Allen, 2002).

The Qoyllur Riti mountain range represents three important tenants in the Sonqueños’ Andean religion: the Riti (the snow), the Taytakuna (the fathers), and the great Apus (Lord Mountains). The rock bearing Christ´s image, now enclosed in a concrete chapel, is a prototype of Sonqo´s own small taytacha—a small portable shrine consisting of a red three-sided wooden box, about one foot square and six inches deep, painted inside with a simple picture of the crucified Christ. Their powerful object, the taytacha, begins with ritual travels within Sonqo, for he is carried around the community for contributions, then visits churches and households. After weeks of preparation, the taytacha sets out on a procession that transcends the community, leading the pilgrims through a landscape of greater and more powerful Places. During Corpus Cristi, the Sonqueños traveling to the glacier peak, carrying the tayacha with them. This ritual allows the Sonqueños to confirm their relationship with the Sacred Places of regional importance and reestablish themselves as an ayllu (Allen, 2002).

The Corpus Cristi exhibits several aspects of both Andean and Catholic religions. The journey itself is described as a pilgrimage to celebrate a Catholic miracle, yet the journey itself is similar to that of the capacocha ceremony: images of the individuals who embody purity and perfection (the Virgin Mary and Jesus Christ) accompany the caravan and are taken to a mountain peak emplaced with both Andean and Catholic sacredness. The Qoyllur Riti mountain range remains to be a sacred site for the Sonqueños, be it similar to that of a Catholic pilgrimage site, or an Andean shrine. The goal of the journey is reestablish the ayllu’s social-economic ties within their community with a particular recognizing their ancient connection to the community’s ancestors, be they abstract ancestors in the afterlife, or the bones in the nearby chullpas, but not, unfortunately, the mummified remains venerated by their Inka forbearers. In sum, the Corpus Cristi ceremony combines both Catholic beliefs and Andean traditions, particularly the use of images of saints and holy individuals in lieu of actual bodies. The Sonqueños thus honor their Inka forbearers while also actively involving Catholic beliefs into their worldview.

Conclusion

In conclusion, the syncretism of Andean religion and Catholicism is apparent in the treatment of the mummified body through time. The perception of the preserved bodies of saints in Catholicism and Andean religion is quite similar in that both religions share similar perceptions on the post-mortem agency and socio-political power the bodies possess. This allowed for the Andean people to both readily accept and quickly modify Catholicism to fit into their ideology. The body, especially the mummified corpse, is therefore a power object that is both maintained and transformed by social and cultural forces in the Andes.

Works cited 

Allen, K. (2002). The Hold Life Has. Smithsonian Institution: Washington D.C.

Andrien, K. (2008). Andean Worlds: indigenous History, Culture, and Consciousness Under Spanish Rule, 1532-1825. Albuquerque: University of New Mexico Press.

Ayala, G. P. Nueva corónica y buen gobierno. (F. Pease, Ed.) Caracas: Biblioteca Ayacucho.

Bauer, B. (1992). Ritual Pathways of the Incas: An Analysis of the Collasuyu Ceques in Cuzco. Latin American Antiquity , 3 (3), 183-205.

Besom, T. (2010). Inka Sacrifice and the Mummy of Salinas Grandes. Latin American Antiquity, 21 (4), 399-422.

Besom, T. (2009). Of Summits and Sacrifice: An Ethnohistoric Study of Inka Religious Practices. Austin : University of Texas Press.

Bynum, C. (1995). Why All the Fuss About the Body? A Medievalist’s Perspective. Critical Inquiry , 22 (1), 1-33.

Ceruti, M. (2003). Llullaillaco: Sacrificios y ofrendas en un santuario inca de alta montaña. Salta: Instituto de Investigaciones de Alta Montanã, Universidad Católica de Salta.

Chamberlain, A. P. (2001). Earthly Remains . New York: Oxford University Press.

Cieza de Leon, P. (1959 [1553]). The Inca of Pedro de Cieza de León. In V. W. Hagen (Ed.), The Inca (H. d. Onis, Trans.). Norman: University of Oklahoma Press.

Cobo, B. (1979 [1653]). History of the Inca Empire . (R. Hamilton, Ed., & R. Hamilton, Trans.) Austin : University of Texas Press.

Cobo, B. (1990 [1653]). Inca Religion and Customs. (R. Hamilton, Ed., & R. Hamilton, Trans.) Austin: University of Texas Press.

Cussen, C. (2005). The Search for Idols and Saints in Colonial Peru: Linking Extirpation and Beatification. Hispanic American Historical Review , 85 (3), 417-448.

Dean, C. (2010). The After-life of Inka Rulers: Andean Death Before and After Spanish Colonization. In J. B. Cortez (Ed.), Death and Afterlife in the Early Modern Hispanic World (pp. 27-54). Hispanic Issues On Line 7.

Dillehay, T. (1995). Introduction. In Tombs for the Living: Andean Mortuary Practices (pp. 1-26). Washington D.C.: Dumbarton Oraks Research Library and Collection.

Doyle, M. (1988). Ancestor Cult and Burial Ritual in the Seventeenth and Eighteenth Century, Central Peru. Los Angeles: Disseratation University of California, Los Angeles.

Duviols, P. (1977). La destrucción de las religiones andinas (conquista y colonia). Mexico D.F.: Universidad Autónoma Nacional de México.

Edwards, P. (1997). A display of faith (religious relics). Practicing Catholic , 62 (1), 1.

Gaither, C., Kent, J., Víctor, V., & and Teresa, R. (2008). Mortuary Practices and Human Sacrifice in the Middle Chao Valley of Pery: Their Interpretation in the Context of Andean Mortyary Patterning. Latin American Antiquity , 19 (2), 107-121.

Geary, P. (1986). Sacred Commodities: the circulation of medieval relics. In A. Appadurai (Ed.), The Social Life of Things: Commodities in cultural perspective (pp. 169-191). Cambridge: Cambridge University Press.

Gose, P. (1994). Deathly Waters and Hungry Mountains: Agrarian Ritual and Class Formation in an Andean Town. Toronto: University of Toronto Press.

Harris, O. (1982). The Dead and the Devils among the Bolivian Laymi. In Death and the Regeneration of Life. Cambridge: Cambridge University Press.

Jeremiah, K. (2012). Christian Mummification: An Interpretative History of the Preservation of Saints, Martyrs and Others. Jefferson : McFarland & Company, Inc.

Linares, E. (1966). Restos arqueológicos en el nevado Pichu Pichu (Arequipa, Perú). Anales de arqueología y etnología , 21, 7-41.

Pearson, M. (2008). The Archaeology of Death and Burial . College Station: Texas A&M University Press.

Pizarro, P. (1978 [1571]). Relación del descunrimiento y conquista del Perú. Lima: Pontificia Universidad Católica del Perú.

Rakita, G., & Buikstra, J. (2005). Introduction. In G. B. Rakita, Interacting with the Dead: Perspectives on Mortyary Archaeology for the New Millennium (pp. 1-14). Gainsville:

University of Florida Press.

Ramos, G. (2010). Death and Conversion in the Andes: Lima and Cuzco, 1532-1670. Notre Dame: University of Notre Dame Press.

Reinhard, J. (1999). Children of Inca Sacrifice Found Frozen in Time . National Geographic , 196 (5), 36-55.

Reinhard, J. (1996). Peru’s Ice Maidens: Unwrapping the Sacrets . National Geographic , 5 (4), 62-81.

Reinhard, J., & Constanza, C. (2000). Investigaciones arqueológicas en el volcán Llullaillaco: Complejo ceremonial incaico de alta montaña. Salta: Universidad Católica de Salta .

Rowe, J. (1995). Behavior and Belief in Ancient Peruvian Mortuary Practice . In Tombs for the Living (pp. 27-42). Washington, D.C.: Dumbarton Oaks Research Library and Collection.

Salomon, F. (1995). “The Beautiful Grandparents”: Andean Ancestor Shrines and Mortuary Ritual as Seen Through Colonial Records. In Tombs for the Living (pp. 355-378). Washington D.C.: Dumbarton Oaks Research Library and Collections.

Salomon, F. A. (1991). The Huarichirí Manuscript, a Testament of Ancient and Colonial Andean Religion. Austin: University of Texas Press.

Sharf, R. (1992). The Idolization of Enlightenment: On the Mummification of Ch’an Masters in Mediveval China. History of Religion , 32 (1), 1-31.

Sillar, B. (1992). Social Life of the Andean Dead. Archaeological review from Cambridge , 11, 107-123.

Sofaer, J. (2008). The Body as Material Culture: A Theoretical Osteoartchaeology. Cambrdige: Cambrdge University Press.

Taylor, G. (1987). Ritos y tradicioines de Huarochirí del siglo XVII. Lima : Instituto de Estudios Peruanos/Instituto Francés de Estudios Andinos, Historia Andina 12.

Tung, T. (2014). Agency, ‘Til Death Do Us Part? Inquiriing about the Agency of Dead Bodies from the Ancient Andes. Cambridge Archaeological Journal , 24, 437-452.

Vago, M. (2007). Piccoli storie di grandi santi [Short histories of great saints]. Rome: Edizioni Messagero.

Vega, G. I. (1966 [1609]). Royal Commentaries of the Incas and General History of Peru: Part One. Austin: University of Texas Press.

Physiological and Evolutionary Mechanisms of Fertility at High Altitude: Part 2

Birth weights, Stillbirth Rates, and Infant Mortality

Exposure to hypoxic environments may increase the stress on an already vulnerable growing fetus, thus result in a higher frequency of low birth weight, higher stillbirths, and increased infant mortality among high altitude populations. Several scholars have reported reduced birth weight with increasing altitude due to inadequate maternal oxygenation later in pregnancy (Yip, 1987; Haas et al., 1977; Ballew and Haas, 1986; Jensen and Moore, 1997; Khalid et al., 1997). For pregnant women, oxygen saturation and hemoglobin concentration naturally decrease towards term, resulting in a fall in arterial oxygen at the end of pregnancy. If a woman is at high altitude, she has even less access to oxygen which may explain the reduction in birth weight at high altitudes (Hartinger et al., 2006).

Hartinger and colleagues (2006) compared birth weights of 84,173 neonates between 1995 and 2002 from the cities of Lima (150 masl), Huancayo (3280 masl), Cusco (3400 masl), and Juliaca (3800 masl). The authors found that birth weight is lower at high altitude, but there is no linear relation between altitude of residence and birth weight (Hartinger et al., 2006). In fact, in Juliaca (3800 m) where the population has resided the longest, birth weight was higher than that of Huancayo (3280 m) where indigenous populations have resided the shortest. In Cusco (3400 m), where there is increased admixture among Spanish and indigenous populations, birth weight was also lower compared to Juliaca (Hartinger et al., 2006). The data suggests that women from families who had lived at high altitudes for at least 3 generations maintained their oxygenation better during pregnancy (McAuliffe, 2001), allowing for a higher birth weight and suggesting that adaptation occurs when groups are exposed to a hypoxic environment over generations (McAuliffe, 2001).

Several studies have confirmed an association between high altitude and a higher stillbirth rate (Gonzales et al., 2007; INEI, 2001) due to an effect of low barometric pressure and colder temperatures common in these hypoxic environments (Gonzales, 2007). For example, populations in the Sarata district of southern Peru almost 20 percent of children do not survive beyond age five (Collins, 1983). Local health personnel and native healers state that the leading cause of infant mortality is respiratory failure, possibly related to the hypoxic environment (Collins, 1983). In fact, respiratory symptoms are reportedly responsible for 58-68 percent of deaths among children under one year of age, and for 49-55 percent of deaths among children aged one to five (Collins, 1983).

To offset the effects of high altitudes, indigenous Peruvian mothers often tightly swaddle and enclose their infants in a set of clothes and blankets, referred to as a manta pouch. The manta pouch modifies the internal microenvironment so that, compared to the ambient environment, the temperature is higher and more stable, the humidity is higher, the partial pressure of oxygen is lower, and stimulation levels are reduced. It appears to be a solution the lower the infant mortality rate among indigenous women (Tronick et al., 1994).

Gonzales and colleagues (2007) compared stillbirth rates from a sample of 22,662 births between 2005 and 2006 for the cities of Lima (150 masl), Huancayo (3280 masl), Cuzco (3430 masl), and Puno (3850 masl), and reported that stillbirth rates were higher at high altitude (>3000m) compared with low altitude (Gonzales et al., 2007). Yet, inhabitants from the South Andes (i.e. Cusco, Puno) actually have lower stillbirth rates compared with the central Andes (Huancayo) (Gonzales et al., 2007). Similar to Passano (1983), Gonzales and colleagues attribute this discrepancy with a vague description of an “ancestry effect,” in which populations with longer multigenerational residence in the southern Andes population may be linked to lower still birth rates (Gonzales et al., 2007).

To summarize, there appears to be no association between an increase in fetal mortality with increasing elevation. High altitudes pose several environmental stressors (e.g. low oxygen and cold temperatures) which increase infant mortality; to counteract these stressors, Peruvian mothers tightly wrap and swaddle their newborns in mantas, creating a protective microenvironment. Interestingly, the rates of perinatal and neonatal mortality are, however, lower in populations that have resided at high altitude for longer; populations inhabiting the southern Andes have a longer antiquity at high altitude and lower rates of fetal and neonatal deaths than those in the central Andes with a shorter residence at high altitude.

Post-Partum Behaviors

Female physiology after birth may contribute to lower fertility levels, but most research has indicated that post-partum behaviors account for a decrease in reproductive rates. The National Institute of Statistics and Informatics of Peru documented longer durations of exclusive breastfeeding at high-altitudes than at sea level as revealed by an increased prevalence of lactation amenorrhea (absence of menstruation)(INEI, 2001). Yet, Gonzales (2007) noted that fertility rates among high altitude populations in Peru are higher compared to those at sea level despite the prevalence of lactation amenorrhea and prevalence of >2 years sexual abstinence after parturition.

Couples living in the Sarata district of Peru take an active role in preventing and regulating births family sizes after reaching the desired number of children size. Collins (1983) reported that women sought herbal specialists who provided herbs, fruits, and seeds thought to induce miscarriages if taken within a month or two of conception. Infanticide is also a common practice, especially if the infant was in some way abnormal, because the harshness of the environment and lack of health care services made the burden of raiding an abnormal or weak child too costly for many families. Other methods approved by the local Catholic nuns included abstinence and the rhythm method. Also, seasonal migration is sometimes prescribed to young couples that were having children more rapidly, and Collins (1983) noted two accounts in which fathers-in-law recommending that their sons–in-law migrate seasonally in order to space births.

Similarly, Laurenson and colleagues (1985) noted that females living in Central Nepal (12,400 feet) experienced lower fertility frequencies than females living at 8500 feet. Though the females at high altitudes reported longer post-partum ammenorhea and breast-feeding periods, the pregnancy gap was due to the later age of marriage and controlled birth spacing (Laurenson, et al., 1985). Overall, it appears that both male and female parents actively seek solutions to control birth spacing in order to achieve desired number of offspring.

Onset of Menopause

Similar to the age of sexual maturation, high altitudes may contribute to an earlier or later onset of menopause. Studies have documented that the age at menopause occurs earlier at high altitude than at sea level (Gonzales, 1994) and therefore result in a shorter reproductive span for women living at altitude (Gonzales and Villena, 1996). Women living at Cerro de Pasco (4340 masl) experienced accelerated menopause compared to women in Lima (150 masl) due to high levels of serum follicle stimulating hormone (FSH) and accelerated oocyte loss observed in regularly menstruating women at high altitude (Gonzales and Gonez, 2000).

Studies have estimated medium age of menopause to be between 45.4 years and 46.1 years among rural Bolivian Aymara, (Crognier et al. 2002; Burch and Vitzthum, 2011). Among women living at high altitude in Nepal, menopause occurs between 45–50 years (Lang and Lang, 1971; Beall, 1983), an age range that is within the average onset of menopause worldwide. Vitzthum (2013) notes, however, that these ranges are similar to those of other populations that have poor living conditions and high mortality risks (e.g., India = 44.0 years; also see Wood, 1994). Like age at menarche, variation in age at menopause may be due to factors other than, or in addition to, hypoxia. Yet, there appears to be little, if any, demographic impact of perhaps a year less at the end of the reproductive life span of women (Vitzthum, 2013).

Evolutionary Mechanisms and Ethnicity/Ancestry Influences on Fertility

Evolutionary processes may have acted differently on the populations who originally migrated into high altitude environments and thus resulted in different patterns of adaptation. These results suggest that longevity of life at high altitude may be an important component of adaptation. For example, the reduced survival of Spanish children at high-altitudes suggests that the newcomers lacked an adaptation to the hypoxic environment (Gonzales, 2007). The indigenous Peruvian population—Aymara and Quechua—was later mixed with the Spaniards who colonized Peru during the 16th century. As a result, the Peruvian population has three important admixture groups: first, the Quechua or Aymara populations with long-term residence in highland zones particularly at the Southern Andes (Cuzco and Puno), and the second is admixture of Spanish with the indigenous Quechua and Aymara populations, and third, the Spanish who moved to high altitude relatively recently in the last four centuries (Rupert and Hochachka, 2001). This introduction and mixture of genes may have stopped or reversed the adaptive processes preformed during more than 10,000 years of life at high altitude. Natives with longer ancestry in high altitudes appear to have an unknown genetic component that make them better adaptive to their environments compared to individuals of Spanish descent.

Evolutionary processes may have acted differently on colonizing populations of the Andes verses those of the Himalayas, resulting in different pattern of adaptation (Beall, 2006). Compared to Andean residents, Tibetans with 20,000 years of antiquity at high altitude demonstrate less intrauterine growth retardation and elevated arterial oxygen content which increases uterus-placental oxygen delivery during pregnancy (Moore et al., 2004; Wiley, 1994). The ability to sufficient deliver oxygen to the fetus and the fetus’ ability to incorporate the oxygen into its system is necessary for the offspring’s survival (Moore et al., 2004; Wiley, 1994).

It appears that a phenotype of high saturation of oxygen may exist among populations with antiquity in high altitude environments. For example, Bealls’ (2006, 2007) research has supported the hypothesis that the higher oxygen saturation allele might be favored by natural selection among Tibetans, but not Andean peoples. To test the hypothesis that high oxygen saturation genotypes have higher Darwinian fitness, Beall (2006, 2007) gathered genealogical, oxygen saturation, and female fertility data from 905 households in 14 villages at 3800-4200 masl in rural areas of the Tibet Autonomous Region and found that infants who were homozygous and heterogygous for oxygen saturation gentoypes had higher likelihood of surviving infancy (Beall 2006, 2007, 2014). This suggests that high-altitude hypoxia acts as an agent of natural selection on the heritable quantitative trait of oxygen saturation via the mechanism of higher infant survival of Tibetan women with high oxygen saturation genotypes (Beall et al., 2004; Beall, 2006, 2007, 2014).

In sum, there are evolutionary forces selected for increased oxygen saturation among Tibetan populations with the greatest antiquity in the Himalayas. Though Andean samples lacked the allele associated with this mechanism, it is possible that similar adaptive forces have been acting on the indigenous populations of the Andes.

Discussion

Historic chroniclers found that indigenous Andean females maintained capacity to reproduce while Spanish colonists were reportedly unable to carry fetus to full term or experienced high infant mortality rates. Low oxygen environments may delay the onset of sexual maturation among Himalayan and Andean populations; however, menarcheal age is well within the range of variation worldwide. Whether or not socio-economic status impacts sexual maturity remains unclear. Overall, it appears to have no demographic consequence because marriage and sexual behaviors typical begin well after puberty between highland Himalaya and Andean populations. Studies documenting gamete formation and testosterone production have demonstrated that exposure to high altitudes negatively impact male reproductively abilities for a short period of time. Mechanisms of ovulation vary between highland and lowland females in both the Andes and Mongolia yet are well within the range of worldwide variation. At times, differential barometric pressures appear to impact female ovulation, but there appears to be no negative impact on female fertility. In fact, it appears that overall health and socioeconomic status may impact overall fertility among high altitude populations. Lower oxygen levels may be linked to lower birth rates among high altitude infants, yet there is no linear relation between altitude of residence and birth weight. In fact, better oxygenation during pregnancy appears to be an adaptation among women with greater ancestral antiquity in high altitudes. Low barometric pressure and cold temperatures are traits of high altitudes and are attributed to the high stillbirth and infant mortality rates. Infants born into populations with greater antiquity in the highlands, however, appear to be more likely to survive compared to infants born to recent immigrants to the highlands. Post-partum behaviors such as breast-feeding, abstinence, herb-inducing miscarriage, and rhythm method, indicate that females actively attempt to regulate reproduction and control birth spacing, thus actively attempt to control their fertility.Variation in age at menopause between highland and lowland populations may be due to hypoxic environments as well as poor living conditions and overall health. However, there appears to be little, if any, demographic impact on the earlier age of menopause among women in high altitudes.

The stressors associated with high-altitude environments impose severe, lifelong stress upon every resident regardless of age, sex, or individual characteristic. Populations living in high-altitude environments do not adapt behaviorally to create non-hypoxic microclimates, people must adapt biologically. In fact, genetic research is beginning to elucidate the how populations with the longest antiquity in high altitudes have certain genes that allow them to live, and thrive, in an otherwise physiological stressful environment.

Conclusion

High altitude environments appear to impact the reproductive physiology of males and females, yet individuals who have a longer ancestry at high altitude appear to have adapted to the low oxygen environments. While socioeconomic factors sometimes negatively impact fertility, it appears that high altitude ancestry appears to have a greater impact on reproductive success. Native populations with a long ancestry in high altitudes have fewer reproductive issues while those who have a mixed ancestry (e.g. Spanish verses Quechua or Aymara; Han Chinese verses Tibetans), are more likely to have issues with fertility. In sum, an examination of fertility in the Andes and Himalaya mountains illuminates complex relationship between proximate behaviors and dynamic evolutionary adaptations which together impact reproductive functioning in high altitude environments.

Physiological and Evolutionary Mechanisms of Fertility at High Altitude: Part 1

High altitudes have the potential to negatively impact normal bodily functions of individuals who are both accustomed, or not properly acclimated, to such environments. Air deficient in oxygen, colder temperatures, greater exposure to solar radiation, and higher energetic costs of subsistence compared to that of lowland environments are potentially detrimental to physiological function. Similarly, high-stress environments with riskier living conditions may lead to economic disparities and locally specific cultural practices. Despite these limitations, human populations have lived, and thrived, in high altitudes environments for thousands of years. I investigate how theses environmental stressors impact reproductive functioning and fertility of indigenous populations living at high altitude, particularly in the Andes and Himalaya Mountains. In particular, I assess whether or not altitude-related stressors and reproductive behaviors contribute to lower fertility rates among high altitude populations. Through analysis of the physiological, behavioral, and genetic properties of males and females living at high attitude, I argue that fertility rates are under strong evolutionary control that offset altitude-induced sicknesses (hypobaric hypoxia) thus limiting variation in fecundity among high altitude populations.

History of the Study of Fertility at High Altitudes

Populations and small-scale societies have a long antiquity at high altitudes, yet much of our early knowledge of whether or not males and females had normal reproductive fitness comes from chronicles written by Europeans colonizing the Andes. Archaeological investigations in the Andes are numerous and are ongoing (Rademaker et al., 2014), yet are still in a very early stage in the Himalaya Mountains (Aldenderfer, 2011). Similarly, studies of the genetic components associated with high-altitude living are novel avenues of investigation among researchers working with populations in both the Andes and Himalayas (Beall, 2006, 2007). Given this incomplete picture, fertility studies conducted among populations living in other high altitudes (e.g. ovulation among Mongolian females) will also be presented when relevant. Because both the Andes and Himalaya Mountains are both extreme high altitude environments, I will explore research on reproductive fitness from both areas while recognizing that the entire picture elucidating the nature of fertility at high altitudes remains incomplete.

It is generally assumed that the human ancestral phenotype of oxygen transport system evolved mainly in environments with normal oxygen levels, or “normoxia” at sea level (Beall, 2006; Hochachka et al., 1998). Geological, vegetational, and archaeological analyses of hominin fossil sites in rift valleys formations in Ethiopia spanning approximately 3 million years indicate that hominid habitation sites were at an altitude of 500-600 meters above sea level (masl), well below an altitude thought to induce hypoxic stress (Bonnefille et al., 2004; Redfield et al., 2003; Quade et al., 2004). Thus, it is assumed that hominid evolution occurred under normoxia, and the corollary that high-altitude hypoxia is a physiological stress seems reasonable (Beall, 2006).

Laguna Cullicocha (4635 masl)

Laguna Cullicocha (4635 masl)

Altitude stress, medically known as hypobaric hypoxia, is cased by the fall in barometric pressure with increasing altitude, resulting in fewer oxygen molecules in a breath of air compared to sea level (Beall, 2006). Barometric pressure decreases with ascending altitude, decreasing oxygen availability in ambient air. Conditions are especially prevalent in the altiplano/puna, a treeless, tundra-like landscape higher than 4000 masl, with little fuel for campsites, and is an area that requires twice the sea-level caloric intake needed to maintain normal metabolic function (Marriot, 1996). Hypobaric hypoxia becomes progressively more severe with increasing altitude and stresses biological systems because a steady, uninterrupted supply of oxygen is required for metabolism in the mitochondria (Beall, 2006). Aside from supplemental oxygen or descent, there is no such strategy to avert the effects of environmental hypoxia (Gonzales, 2007; Julian, 2011). Though hypobaric hypoxia is the most pervasive physiologic challenge associated with high-altitude exposure, lower humidity, colder temperatures, increased solar radiation, and high energetic costs of subsistence that also accompany higher elevations may also threaten physiological well-being and reproductive behavior (Baker and Little, 1976).

Despite these stressors, human populations have occupied high altitudes for thousands of years. Archaeologists have uncovered ample evidence of human residency in high altitude environments as early as 20,000 years ago (Rademaker et al., 2014). The Tibetan Plateau of the Himalaya Mountains exhibits archaeological evidence of worked stone (Aldenderfer, 2011) and handprints and footprints (Quesang site) at 4200 masl (Zhang et al., 2002). Butchered animal bones, stone artifacts, and small-scale hearths dating from 14,600 to 7500 calendar years before the present (cal yr B.P.) at Jiangxigou 1 (~3200 masl); Heimahe 1 (~3200 masl) (Brantingham and Gao, 2006); at Xidatan 2 (~4300 masl) (Brantingham et al., 2013); and at Yeniugou (3800 masl) in the northeastern part of the plateau (Tang et al., 2013).

Tibetan Plateau (approx 4500 masl)

The earliest archaeological evidence of human occupation in the South American Andes dates to as early as 10,000 to 12,000 years BCE (Rademaker et al., 2014; Bonavia, 1991). The Pucuncho Basin in the southern Peruvian Andes contains the highest-altitude Pleistocene archaeological sites yet identified in the world (4355 masl) dating to 12,800-11,500 (Rademaker et al., 2014). Additional evidence of human occupation above 4000m of altitude with an antiquity of 10,000 years also has been found at the sites of Lauricocha, Huanuco (3850m) (Cardich, 1960) and Telarmachay, San Pedro de Cajas (4400m) in the Peruvian Andes (Bonavia, 1991).

Spanish chroniclers began to note the effect high altitude environments in the Andes had on living organisms during the 16th and 17th centuries early after colonization of the New World. Conquistadors such as Cieza de Leon (1553) described much about life among the Inca during the Spanish conquest and noted that the Inca had a surprisingly high fecundity rate. It was evident that Spaniards could produce offspring up to 3400 masl, yet infertility and stillbirths were frequent among Spaniards living in settlements around and above 4000 masl (Gonzales, 2007). Early chroniclers such as de la Vega and Cobo were of the opinion that the altitude effects on organisms were mainly attributable to the cold (de la Vega, 1609; Cobo, 1653). De la Calancha (1639) remarked in his chronicle that in Potosi (4300 m), in modern-day Bolivia, the natives had normal fertility and the offspring survived, whereas Spaniards encountered problems in having descendants. In fact, it was not until 53 years after then Spaniards settled the Andes did de la Calancha (1639) describe the birth and survival of the first child from two Spaniards in Potosi (4300 masl). Overall, chroniclers found that indigenous Andean females maintained capacity to reproduce while Spanish colonists were reportedly unable to carry fetus to full term or experienced high infant mortality rates.

Drawing by Guaman Poma de Ayala (1615/1616)

Given the discrepancy of fertility rates between newcomers to the Andes and the indigenous peoples, local biologists, biological anthropologists, and geneticists began to investigate the manner in which high altitude environments impact reproduction. Yet, many studies tend to produce contradicting results. The first fertility studies investigated the effects of altitude on fertility among sheep, cattle, cats, and rabbits, and demonstrated that short-term exposure to high altitude resulted in temporary infertility (Monge, 1942, Monge and Mori- Chávez, 1942; Monge et al., 1945).Studies in the late 20th century have shown that fertility is lower in the economically underdeveloped areas of the Andes than in the more prosperous Spanish-speaking parts (Collins, 1983). Studies documenting the fecundity rate (as calculated by the number of viable offspring per female) among Peruvian highlanders has found to be from one to two births less than that of lowland Peruvians of the same ethnic background. In fact, highland natives who move to low altitudes show markedly higher rates of fertility than their counterparts who remain in the highlands (Abelson, 1976). Conversely, studies have also noted that population fertility appears to be unaffected among natives to high altitude environments (Hoff, 1984). A retrospective hospital-based study performed on women of La Paz (3600 m), Bolivia shows that high altitude does not impair fertility (Suarez-Morales, 1967). In fact, the number of viable offspring born per female in the Andes has also been documented to be higher amongst high-altitude populations compared to those at sea level, suggesting that high altitude does not reduce fecundity in human populations (Gonzales, 2007). Additionally, scholars have noted that highlanders of both the Andes and Himalayas have distinctive morphological and physiological characteristics that seemed adaptive in the sense that they might offset hypoxia stress (Baker and Little, 1976; Monge, 1978). Given the complex and sometimes conflicting nature of the fertility data, considerations of the physiological mechanisms of reproduction as well as behavioral and genetic profiles will elucidate the nature of fertility at high altitudes.

Physiological and Behavioral Impacts on Fertility and Reproduction

At high altitude, the oxygen transport system must offset ambient hypoxia in order to maintain tissue oxygen levels to support maintenance, growth and development, and reproduction. Altitude-induced stress, hypoxia in particular, may act to affect the process of reproduction at several stages: formation of gametes and gametogenesis, the ovarian cycle and menstruation, birth weights, still birth rates, infant mortality, post-partum behaviors, and age of menopause.  Assessing how hypoxic stress impacts fertility alone is problematic because fertility is also affected by many cultural, social, and behavioral factors. Populations residing at high altitudes may have less developed health, social, and communication infrastructures than those residing at sea level. These reproductive categories will be explored while considering socioeconomic disparities and cultural practices impacting fertility. Over the next few weeks, I will address each of these reproductive systems beginning with development and formation of gametes and testosterone levels.

Development and Formation of Gametes and Testosterone Levels

Delay in the development of and abnormal formation of gametes may also impact fertility. In particular, research has documented whether or not male reproductive functions are negatively affected during and after high altitude sojourns. Early studies conducted on guinea pigs taken to Morochocha, Peru (4500m), observed degenerative alterations in the seminiferous tubules, which serve a crucial role in the production of male gametes (Guerra-Garcia, 1959).

Exposure to hypoxia and physical stress of high altitudes may induce reversible spermatogenic and/or Leydig cell dysfunction, a condition that decreases testosterone production (Saxena, 1995). Analysis of gamete production conducted on three subjects who trekked for 21-24 days between 5100-6700 masl revealed an increased rate of abnormal sperm shape (Abramsson et al., 1982), which would present an important problem if the subjects wanted children (Okumura et al., 2003). Additionally, scholars have observed that sperm counts had not recovered 3 months after subjects returned from the expedition. Yet, all subjects had normal gamete production and formation after 2 years (Okumura et al., 2003). Okumura and colleagues (2003) also observed an increase in abnormally shaped sperm 1 month after the subjects returned to sea level. Sperm shape had nearly recovered to the pre-expedition state after 3 months (Okumura et al, 2003).

Mount Everest (8848 masl)

In addition to hypoxia, physical stress while trekking and carrying heavy loads may also contribute to the initial decline in testosterone levels (Okumura et al., 2003). Endocrine tests conducted on the three subjects revealed slightly lower levels of testosterone in the blood 1 month after the expedition and decreased still further after 3 months. After 2 years, testosterone levels were normal. The subjects in the study also complained of erectile dysfunction after returning from the expedition, which may have been partly due to decreased testosterone (Okumura et al., 2003).

Semen analysis and recorded reproductive hormone levels taken from seven male mountaineers trekking through the Himalayas (approximately 5900 masl) found that physical exercise at high altitudes is associated with a testicular dysfunction leading to a reduced sperm concentration probably through an altered spermiation (Pelliccione et al., 2011). Interestingly, the physical exercise improved the male’s overall body composition, which increased testosterone levels after the expedition (Pelliccione et al., 2011).

In sum, studies have demonstrated short-term exposure to high altitudes negatively impact male gamete formation and testosterone production, ultimately affecting his ability to reproduce. It should be noted, however, that male gametes production and testosterone levels return to normal once he returns to sea level for several months to 1-2 years.

These are very high altitudes where people do not reside. Historically and in the archaeological record, however, there is evidence that people would take occasional sojourns to high mountain summits in the Andes. Spanish chronicler Cobo (1653) described how the Inka embarked on ritual pilgrimages (qhapaq huachas) to mountain summits were they would leave female and male children of exemplary physical perfection as immolate tribute to the Inka Empire and mountain gods. Freeze-dried bodies of these sacrificed children have been recovered from mountain summits up to 5200 masl in Chile, Argentina, and Peru (Reinhard and Ceruti, 2000). Physiologically, even brief sojourns to extreme altitudes has a minor impact on the reproductive system.

Ovarian Cycle and Menstruation

Ovulatory disorders are a major cause of infertility (Urman et al., 2006). While follicle phase ranges vary among women, a luteal phases lasting for less than 2 weeks is considered a “luteal defect” due to low levels of the hormone progesterone and an insufficient production of uterine lining, which inhibits a female’s reproductive abilities. Fecundability may be correlated to cycle length, which determines the number of opportunities for conception in a given time span (Wood and Weinstein, 1988). Because ovarian follicle growth is characterized by cell growth and rapid cell divisions, hypothetically, hypoxia may slow this process and thereby disrupt phase lengths (Wood and Weinstein, 1988).

Recent studies have suggested that short-term exposure to high-altitude hypobaric hypoxia may negatively impact the development and function of the corpus luteum. Parraguez and colleagues (2013) examined the corpus luteum among sheep living in high altitudes and found a significant decrease the growth and function of the corpus luteum, which resulted in decreased fertility (Parraguez et al., 2013). However, it is important to note that sheep used in the study were Creole ewes, a mixed breed developed from Churra and Manchega Spanish breeds brought to the Americas by Spanish colonists and therefore do not have a long ancestry in high altitude environments (Parraguez et al., 2013).

Among indigenous Aymara women on the altiplano (3800+ masl) of the Peruvian and Bolivia Andes, Vitzthum and colleagues (2000) reported a mean cycle length of 29.1 days (n = 612 cycles, 191 women). Cycle length among nomadic herders from the Mongolian high steppe (~1,500 masl) was 27.8 days, with the mean follicular-phase length averaging 14.7 days, and mean luteal-phase length 13.2 days (Jurado et al., 2009). According to Vitzthum (2009), neither the Aymara nor Mongolian cycle ranges were particularly low or high compared to cycle length of female populations worldwide. If hypoxia does slow follicle growth, the effect is insignificant (Vitzthum, 2013).

Differential hormone profiles, specifically time between the gonadotropin peak/release of luteinizing hormone (LH) and ovulation, between high and low altitude populations may indicate an ovulatory disorder. Escudero et al. (1996) compared samples from Lima (150 m) (N=10) and Cerro de Pasco (4340) (N=10), Peru. Females in Cerro de Pasco had smaller pre-ovulatory follicle diameters and lower estrogen production during the late follicle phase. Estradiol levels only increased 80% between Cerro de Pasco females compared to 137.3% among females in Lima. Additionally, the luteinizing hormone peaked earlier among women in Cerro de Pasco compared to women in Lima. Yet, both groups of females exhibited the same duration of the luteal phase and the same endometrium measurements between high and low altitudes (Escudero et al., 1996). Escudero and colleagues (1996) conclude that the differences in hormone profiles during menstrual cycle between high altitude and sea level samples are a result of low barometric pressure.

Conversely, Vitzthum and colleagues (2001a) compared ovulation rates between indigenous “middle-class” women in La Paz (3650 masl), Bolivia, and rural women living outside La Paz in El Alto (4150 masl), and reported that the rural participants had lower ovulation rates compared to the urban middle-class women, indicating that the difference in ovulation rates is not attributed to hypoxia because the two samples reside at similar altitudes (Vitzthum et al., 2001a, 2009). It is possible that overall health and socioeconomic status may impact overall fertility, yet the differences in ovulation lengths between the middle class and rural women may reflect normal variation (Vitzthum et al., 2001). The differences in ovulation may be correlated to socioeconomic status; ultimately, however, the high altitudes and sea level samples fall within the normal ranges of phase length and do not negatively impact reproduction.

Works cited in Parts 1 and 2 

Abelson, A.E. (1976). Altitude and fertility, Anthropological Studies of Human Fertility, ed. Bemice Kaplan, Detroit, 83-92.).

Abramsson, L.; Beckman, G.; Nordenson, I. (1982). Chromosomal aberrations and male infertility. J. Urology, 128, 52–53.

Aldenderfer, M. (2011). Peopling the Tibetan plateau: Insights from archaeology. High Altitude Medical Biology, 12, 141-147.

Baker, P.T. and Little, M.A. (1976). Man in the Andes: A multidisciplinary study of high-altitude quechua: US/IBP Synthesis Series 1. Dowden, Hutchinson and Ross, Inc., Stroudsburg, PA.

Beall, C.M. (2007). Detecting natural selection in high-altitude human populations. Respiratory Physiology and Neurobiology, 158, 161-171.

Beall, C.M. (2006). Andean, Tibetan, and Ethopian Patterns of Adaptaiton to High-Altitude Hypoxia. Integrative and Comparative Biology, 46, 18-24.

Beall, C.M. (1983). Ages at menopause and menarche in a high-altitude Himalayan population. Annual Human Biology, 10, 365-370.

Beall, C.M., Kijoung, S.; Elston, R.C.; Goldstein, M.C. (2004). Higher offspring survival among Tibetan women with high oxygen saturation genotypes residing at 4,000 m. Proceedings for the National Academy of Science, 101, 14300-14304.

Ballew, C.; Haas, J.D. (1986) Altitude difference in body composition among Bolivian newborns. Human Biology, 58, 871-882.

Bonavia, D. (1991). Peru. Man and History. From the Origin to Century XV, first ed. Edubanco, Lima, 586.

Bonnefille, R.; Potts, R.; Chalie, D.; Jolly, D.; Peyron, O.; (2004). High-resolution vegetation and climate change associated with Pliocene Australopithecus afarensis. Proceedings for the National Academy of Science, U.S.A., 101, 12125-12129.

Brantingham, P.J.; Xing, G., Madsen, D.B.; Rhode, D.;  Perreault, C.; van der Woerd, J.; Olsen, J.W. (2013). Late occupation of the high-elevation Northern Tibetan Plateau based on cosmogenic, luminescence, and radiocarbon ages. Geoarchaeology 28, 413–431.

Brantingham, P.J. and Gao, X. (2006). Peopling of the northern Tibetan Plateau. World Archaeology, 38, 387–414.

Burch, J.C.; Vitzthum, V.J.; (2011). Project REPA: the timing of menopause in a population with high mortality risks. American Journal of Human Biology, 23, 254.

Cardich, A. (1960). Investigaciones prehistoricas en los Andes peruanos. In: Antiguo Peru: Espacio y Tiempo. Libreria Editorial Juan Mejia Baca, Lima, 89-118.

Cieza de Leon, P. (1553). Cronica del Peru. Book 2. Sevilla, Spain.

Cobo, B. (1653). Historia del Nuevo Mundo. Imprenta E. Rasco, Sevilla, Spain.

Collins, J.L. (1983). Fertility Determinants in a High Andes Community. Population and Development Review, 9, 61-75.

Crognier E.; Villena, M.; Vargas, E.; (2002). Reproduction in high altitude Aymara: physiological stress and fertility planning? Journal of Biological Science, 34, 463–473.

De La Calancha, A. (1639). Cronica Moralizadora de la Orden de San Augstin Imprenta Pedro Lacaballeria, Barcelona, Spain.

De la Vega, I.L. (1609). Comentarios Reales. Two Books. Merurio, Lima.

Escudero, F., Gonzales, G.F., Gonez, C. (1996). Hormone profile during the menstrual cycle at high altitude. International Journal of Gynecology and Obstetrics, 55, 49-58.

Giussani, D.A.; Phillips, P.S.; Anstee, S.; Barker, D.J.P.; (2001). Effects of altitude versus economic status on birth weight and body shape at birth. Pediatric Research, 49, 490–494.

Goldstein, M.C., Tsarong, P., Beall, C.M., (1983). High Altitude Hypoxia, Culture, and Human Fecundity/Fertility: A Comparative Study. American Anthropologist, 58, 28-39.

Gonez, C.; Villena, A.; Gonzales, G.F. (1993). Serum levels of adrenal androgens up to adrenarche in Peruvian children living at sea level and at high altitude. Journal of Endocrinology, 136, 517.

Gonzales, G.F. (2007). Peruvian contributions to the study on human reproduction at high altitude: From the chronicles of the Spanish conquest to the present. Respiratory Physiology and Neurobiology, 158, 172-177.

Gonzales, G.F. (1998). Demographic, reproductive, morbidity and mortality patterns at high altitude. In: Ohno, H., Kobayashi, T., Masuyama, S., Nakashima, M. (Eds.), Progress in Mountain Medicine at High Altitude, Japanese Society of Mountain Medicine, Tokorosawa, 174–179.

Gonzales, G.F. (1994). Studies on menopause in Peru. Acta Andina, 3, 55-70.

Gonzales, G.F., Tapia, V., Carrillo, C.E. (2007). Stillbirth rates in Peruvian populations at high altitude. International Journal of Gynecology and Obstetrics, 100, 221-227.

Gonzales, G.F. and Gonez, G. (2000). High serum follicle stimulating hormone (FSH) during perimenopause at high altitude, International Journal of Gynecology & Obstetrics, 68, 158-161.

Gonzales, G.F. and Villena, A. (1997). Age at menopause in central Andean Peruvian women, Menopause, 4, 32–38.

Gonzales, G.F., Villena, A., Ubilluz, M. (1996). Age at Menarche in Peruvian Girls at Sea Level and at High Altitude: Effect of Ethnic Background and Socioeconomic Status. American Journal of Human Biology, 8, 457-463.

Gonzales, G.F.; Ortiz, I. (1994) Age at menarche at sea level and high altitude in Peruvian women of different ethnic backgrounds. American Journal of Human Biology, 6, 637-640.

Gonzales, G.F., Guerra-Garcia, R., (1993). Algunas caracteristicas del embarazo y del recien nacido en la altura. In: Leon-Velarde, F., Arregui, A. (Eds.), Hipoxia: investigaciones basicas y clinicas. Homenaje a Carlos Monge Cassinelli. Instituto Frances de Estudios Andinos and Universidad Peruana Cayetano Heredia, Lima, 321–337

Greksa, L.P. (1990). Age of menarche in Bolivian girls of European and Aymara ancestry, Annual Human Biology, 17, 49–53.

Gupta, R.; Basu, A.; Pawson, I.G.; Bharati, P.; Mukhopadhyay, B.; Mukhopadhyay, S.; Roy, S.K.; Majumder, P.P.; Bhattacharya, S.K.; Bhattacharya, K.K.; Das, S.K. (1989) Altitude and human biology: a comparative study of Himalayan, Andean and Ethiopian data. In; Basu, A.; Gupta, R. ed. Human biology of Asian highland population in the global context. Calcutta: Indian Anthropological Society, 1-80.

Guerra-Garcia, R.; Velasquez, A.; Whittembury, J. (1965). Urinary testosterone in high altitude natives. Steroids, 6, 351–355.

Hartinger, S., Tapia, V., Carrillo, C., Bejarano, L., Gonzales, G.F. (2006). Birth weight at high altitudes in Peru. International Journal of Gynecology and Obstetrics, 93, 275-281.

Haas, J.D., Baker. P.T.; Hunt, E.E. (1977) The effects of high altitude on body size and composition of the newborn infant in southern Peru. Human Biology, 49, 611-628.

Hochachka, P.W.; Gunga, H.C.; Kirsch, K. (1998). Our ancestral physiological phenotype: An adaptation for hypoxia tolerance and for endurance performance? Procedures for the National Academy of Science, U.S.A., 95, 1915-1920.

INEI, (2001). Encuesta Demogra ́fica y de Salud Familiar (Peru). 2000. Instituto Nacional de Estadística e Informatíca, Lima, Perú

Jensen, G.M.; Moore, L.G. (1997) The effect of high altitude and other risk factors on birth weight: independent or interactive effects? American Journal of Public Health, 87, 1003-1007.

Julian, C.G. (2011) High Altitude During Pregnancy. Clinics in Chest Medicine, 32, 21-31.

Jurado, K.; Vitzthum, V.J.; Deimel, C.; Deschner, T. (2009). Does high animal fat and protein consumption alter the duration of ovarian cycle phases? Evidence from a study of nomadic Mongolian herders, American Journal of Human Biology, 21, 258.

Khalid, M.E., Ali, M.E.; Ali, K.Z. (1997) Full-term birth weight and placental morphology at high and low altitude. International Journal of Gynecology and Obstetrics, 57, 259-265.

Lang, S.D.R. and Lang, A. (1971). The Kunde hospital and a demographic survey of the Upper Khumbe, Nepal. New Zealand Medical Journal, 74, 1-8.

Laurenson, I.F.; Benton, M.A.; Bishop, A.J.; Mascie-Taylor, C.G.N (1985). Fertility at low and high altitude in central Nepal. Social Biology, 32, 65–70.

Marriot, B.M., and Carlson-Newberry, S.J., (1996). Nutritional Needs in Cold and High Altitude Environments: Applications for Military Personnel in Field Operations, National Academy Press, Washington, D.C.

Mazess, R.B.; (1965). Neonatal mortality and altitude in Peru. American Journal of Physical Anthropology, 23, 209–213.

McAuliffe, F.; Kametas, N.; Krampl, E.; Ernsting, J.; Nicolaides, K. (2001). Blood gases in pregnancy at sea level and at high altitude, International Journal of Obstetrics & Gynaecology, 108, 980–985.

Monge, M.C. (1978). Acclimatization in the Andes. Reissued 1948 edition. The Johns Hopkins Press, Baltimore.

Monge, M.C. (1942). Fisiologia de la reproduccion en la altura. Aplicaciones a la industria animal. An. Fac. Med. Lima, 25, 19.

Monge, M.C.; San Marin, M.; Atkins, J.; Casanon, J. (1945). Aclimatacion del Ganado ovino en las granes Alturas. An. Fac. Med. Lima, 28, 15.

Monge, M.C. and Mori-Chavez, P. (1942). Fisiologia de la reproduccion en la altura. An Fac. Med. Lima 25, 34-40.

Moore, L.G.; Young, D.A.; McCullough, R.E.; Droma, T; Zamudio, S. (2001). Tibetan protection from intrauterine growth restriction (IUGR) and reproductive loss at high altitude. American Journal of Human Biology, 13, 635–644.

Myres, J.E.; Malan, M.; Shumway, J.B.; Rowe, M.J.; Amon, E.; Woodward, S.R.; (2000). Haplogroup-associated differences in neonatal death and incidence of low birth weight at elevation: a preliminary assessment. American Journal of Obstetrics and Gynecology, 182, 1599-1605.

Okumura, A., Fuse, H., Kawauchi, Y., Mizuno, I., Akashi, T. (2003). Changes in Male Reproductive Function after High Altitude Mountaineering. High Altitude Medicine and Biology, 4, 349-353.

Parraguez, V.H.; Urquieta, B.; Pérez, L.; Castellaro, G.; De los Reyes, M.; Torres-Rovira, L.; Aguado-Martínez, A.; Astiz, S.; González-Bulnes, A. (2013). Fertility in a high-altitude environment is compromised by luteal dysfunction: the relative roles of hypoxia and oxidative stress Reproductive Biology & Endocrinology. 11 1-12.

Passano, S. (1983). Caracteristicas de las gestantes y de los recien nacidos en Puno 3812m, Doctoral Thesis, Universidad Peruana Cayetano Heredia, Lima, Peru

Pelliccione, F.; Verratti, V.; D’Angeli, A.; Micillo, A.; Doria, C.; Pezzella, A.; Iacutone, G.; FFrancavilla, F.; di Guulio, C.; Francavilla, S. (2011). American Society for Reproductive Medicine, 96, 28-33.

Quade, J.; Levin, N.; Semaw, S.; Stoug, D.; Renne, P.; Rogers, M.; and Simpson, S.; (2004). Paleoenvironments of the earliest stone toolmakers. Gona, Ethiopia. GSN Buletin, 116, 1529-1544.

Rademaker, K.; Hodgins, G.; Moore, K; Zarrillo, S.; Miller, C.; Bromley, G.R.M.; Keach, P.; Reid, D.A.; Alvarez, W.Y.; Sandweiss, D.H. (2014) Science, 346, 466-469.

Redfield, T.F.; Wheeler, R.H.; and Often, M. (2003). A kinematic model for the development of the Afar Depression and its paleogeographic implications. Earth and Planetary Science Letters, 216, 383-398.

Rimpela, A.H. and Rimpela. M.K. (1993). Towards on equal distribution of health? Socioeconomic and regional differences of the secular trend of the age of menarche in Finland from 1979 to 1989. Acta Paediatr, 82, 87-90.

Rupert, J.L.; Hochachka, P.W. (2001). Genetic approaches to understanding human adaptation to altitude in the Andes. Journal of Experimental Biology, 204, 3151–3160.

Saxena, D.K. (1995). Effect of hypoxia by intermittent altitude exposure on semen characteristics and testicular morphology of male rhesus monkeys, International Journal of Biometeorology, 38, 137–140.

Sobrevilla, L.A. (1971). Nacer en los Andes. Estudios fisiologicos sobre el embarazo y parto en la altura. Doctoral Thesis, Universidad Peruana Cayetano Heredia: Instituto de Investigaciones de la Altura, Lima, Peru 1997

Suarez-Morales, R. (1987). Fertilidad en la altura. Prensa Med. (Bolivia), 19, 79-85.

Tang, H.S.; Zhou, C.L.; Li, Q.Y.; Liang, Z. (2013) A new discovery of microlithic information at the entrance to the Northern Qingzang Plateau of the Kunlun Mountains of Qinghai. China Science Bulletin, 58, 247–253

Tronick, E.Z.; Thomas, R.B.; Daltabuit, M. (1994). The Quechua Manta Pouch: A Caretaking Practice for Buddering the Peruvian Infant against the Multiple Stressors of High Altitude, Child Development, 65, 1005-1013.

Urman, B; Yakin, K; (1988). Ovulatory disorders and infertility, Journal of Reproductive Medicine, 51, 267-283

Vitzthum, V.J. (2013). Fifty Fertile Years: Anthropologists’ Studies of Reproduction in High Altitude Natives. American Journal of Human Biology, 25, 179-189.

Vitzthum, V.J. (2009). The ecology and evolutionary endocrinology of reproduction in the human female, American Journal of Physical Anthropology, 140 (Suppl 49), 95–136.

Vitzthum, V.J.; Wiley, A.S. (2003). The proximate determinants of fertility in populations exposed to chronic hypoxia, High Altitude Medical Biology, 4, 125–139.

Vitzthum, V.J. (2001a). Why not so great is still good enough: flexible responsiveness in human reproductive functioning, In: Ellison PT, edi. Reproductive ecology and human evolution, New York: Aldine de Gryter, 179–202.

Vitzthum, V.J. (2001b). The home team advantage: reproduction in women indigenous to high altitude, Journal of Experimental Biology, 204, 3141–3150.

Vitzthum, V.J.; Spielvogel, H.; Caceres, E.; Gaines, J.. (2000). Menstrual patterns and fecundity in non-lactating and lactating cycling women in rural highland Bolivia: Implications for contraceptive choice. Contraception, 62, 181-7.

Weitz, C.A.; Pawson, I.G.; Weitz, M.V.; Lang, S.D.R.; Lang, A. (1978). Cultural factors affecting the demographic structure of a high altitude Nepalese population, Social Biology, 25, 179-195.

Wiley, A.S.; (1994). Neonatal and maternal anthropometric characteristics in a high altitude Himalayan population, American Journal of Human Biology, 6, 499–510.

Wood, J.W. (1994). Dynamics of human reproduction. New York: Aldine de Gruyter.

Wood, J.W.; Weinstein, M. (1988). A model of age-specific fecundability, Population Studies, 42, 85–113.

World Health Organization (WHO) (1986) World Health Organization Multicenter study on menstrual and ovulatory patterns in adolescent girls: I.A. multicenter cross-sectional study of menarche, Journal of Adolescent Health Care, 7, 229-235.

Yip, R. (1987) Neonatal size and infant mortality at high altitude in the western
Himalaya. American Journal of Physical Anthropology. 94, 289-305.

Zhang, D.D. and Li, S.H. (2002) Optical dating Optical dating of Tibetan human hand- and footprints: An implication for the palaeoenvironment of the last glaciation of the Tibetan Plateau. Geophysical Research Letter, 29, 16-1–16-3.

Forensic anthropology Methodologies: Excavations of Mass Grave sites with Comingled Skeletonized Remains

This week I will explore how forensic anthropologists determine whether or not a human rights violation occurred by utilizing particular techniques developed by forensic practitioners as well as interdisciplinary methods used by archaeologists. Forensic archaeologists employ a variety of methods when excavating mass graves, paying particular attention to whether or not individuals were buried or reburied multiple times by examining the placement and position of the victims’ remains, the associated artifacts, and taphonomic changes to the bone. Collection of evidence and detailed description of mass graves are necessary to reconstruct the events that transpired and ultimately to prosecute the alleged perpetrators of war crimes, crimes against humanity, and genocide.

Forensic teams investigating human rights violations enlist the help of a forensic archaeologist, who is trained in identifying how a gravesite was formed, filled, and concealed, along with taphonomic alterations to the gravesite and the humans remains.

There are several questions a forensic archaeologist must answer while excavating mass grave sites

How many bodies it takes to constitute a “mass” grave?

-Need only two or more bodies

-Actual examples in Croatia created after the disintegration of the former Yugoslavia: 3-750 bodies

-Yet, a grave containing one individual does not necessarily mean that a human rights violation did not occur

So what constitutes a “mass” grave? 

Main definitive factor: nature of the body deposition and manner of which bodies were handled that reflect disrespect. They are distinct from other mass burials in which bodies are carefully placed, indicating a degree of care or at least forethought

How do forensic teams describe gravesites? Is there a gravesite typology?

There is a general typology forensic archaeologists follow when identifying, describing, and excavating mass gravesites

Execution site: location in which multiple individuals are executed; possibly see skeletal materials, bullet cartridges, shredded clothing, human blood and tissue fragments visible on either the ground surface or obscured by grave put or a similar feature intended to inter the human remains and other relevant evidence of a crime

Temporary surface deposition sites: characterized by the presence of residual clothing, personal effects, blood, and bone fragments; the body or bodies were once at this site, and then moved to another location after execution, possibly in an attempt to better hide the crime. Skeletal remains may exhibit taphonomic changes (i.e. weathering, sun-bleaching, insect cases, carnivore damage).

Primary inhumation site: An intentionally constructed pit in which to dispose bodies; typically contains multiple individuals who have been executed and interred soon after death and who share a related cause and manner of death; note that the PIS may be located far from where the victims were killed; human remains disposed in a disorderly manner and associated with evidence of execution, such as bullets and shrapnel; there should be no taphonomic changes, as there should have been no disruption of the natural decomposition process (expect to see “feather-edging” when the peripheral bodies of the bod mass are less preserved than those in the core of the assemblage)

Secondary inhumation site: Remains are removed from the primary inhuman site and moved to a clandestinely created grave; typically, transporting the materials usually results in disarticulation of the skeletal resulting in a disarticulated and commingled remains in a secondary inhumation site

Robbed or looted inhumation sites: Once the remains have been removed from a primary inhumation gravesite, the gravesite is then defined as a “robbed or looted inhumation site.” Usually the perpetrators clandestinely remove the remains for the purpose of creating a secondary inhumation site known to a minimum number of informants. The RLIS will include: clothing, hair, ballistics, and other items small enough to be left behind

This type of grave in particular is important to international tribunals because it assists in linking and reconstructing the sequence of events experienced by the victims

How do forensic archaeologists handle skeletonized human remains?

An additional goal is to maximize collection of disarticulated and commingled skeletal remains in the best possible condition

There are two primary excavation methods: pedestaling and stratigraphic, or “basin” method. The pedestal method focuses on exposing the body or bodies; stratigraphic, or basin method in which the excavator maintains the integrity of the grave features (i.e. grave walls) and its contents

Tuller and Duric (2006) found that the stratigraphic method 1.) had a lower number of unassociated bones; 2.) better maintained the provenience and articulation of remains and 3.) higher recovery rate of smaller bones compared to the team using the pedestal method

Case Study: “Ethnic Cleansing” of Northwestern Bosnia

The anthropological protocol implemented during the investigation mass graves is illustrated from the excavations of mass graves from the “ethnic cleansing” of Northwestern Bosnia in 1992. Hundreds of individuals were disposed in an open cast mine in Northwest Bosnia after being removed by a mechanical excavator from a primary burial site. The perpetrators relocated the remains to a new site, an open cast mine in northwestern Bosnia, and were not particularly systemic or careful with the exhumation, resulting in unnecessary disarticulation of the remains (Baraybar and Gasior, 2006). In the second burial site, one of the walls in the pit was blown up with explosives, causing an avalanche of rubble and rocks that covered the slope, which damaged and caused mixture of the bodies (Baraybar and Gasior, 2006). When the Bosniak Commission on Missing Persons excavated the bodies in 2001, it was crucial for the forensic practitioners to recognize that the final burial site was, in fact, not the primary burial pit and that the remains were interred multiple times and were even subject to taphonomic changes not related to the actual crime (Baraybar and Gasior, 2006). Additionally, the stratigraphic, “basining” excavation method of the primary burial site revealed that the grave pit itself was man-made, suggesting that the disposal of the individuals was premeditated and the perpetrators attempted to hide their transgression (Baraybar and Gasior, 2006).

In sum, archaeological field methods combined with the goals of forensic anthropology specialty affords practitioners and individuals investigating crimes against humanity the opportunity to scientifically investigate mass gravesites. Reconstructing the events that transpired and determining whether or not a mass killing was premeditated together may provide strong evidentiary support for a crime against humanity.

See articles for more information: 

Baraybar, P., & Gasior, M. (2006). Forensic Anthropology and the Most Probable Cause of Death in Cases of Violations Against International Humanitarian Law: An Example from Bosnia and Herzegovina. Journal of Forensic Science , 51 (1), 103-108.

Jessee, E., & Skinner, M. (2005). A typology of mass grave and mass grave-related sites. Forensic Science International , 152, 55-59.

Schmitt, S. (2002). Mass graves and the collection of forensic evidence: genocide, war crimes and crimes against humanity. In W. Haglund, & M. Sorg (Eds.), Advances in Forensic Taphonomy: Method, Theory and Archaeological Perspectives (pp. 277-292). New York: CRC Press.

Skinner, M. (1987). Planning the archaeological recovery of evidence from recent mass graves. Forensic Science International , 34, 267-287.

Skinner, M., Alempijevic, D., & Djuric-Srejic, M. (2003). Guidelines for international forensic bio-archaeology monitors of mass grave exhumantions. Forensic Science International , 134, 81-92.

Tuller, H., & Duric, M. (2006). Keeping the pieces together: Comparions of mass grave excavation methodology. Forenic Science International , 156, 192-200.

the individuals was premeditated and the perpetrators attempted to hide their transgression (Baraybar and Gasior, 2006).

In sum, archaeological field methods combined with the goals of forensic anthropology specialty affords practitioners and individuals investigating crimes against humanity the opportunity to scientifically investigate mass gravesites. Reconstructing the events that transpired and determining whether or not a mass killing was premeditated together may provide strong evidentiary support for a crime against humanity.

Anatomy and Behavioral Strategies of Human and Nonhuman Primate Parturition

In March of 2000, Sofia Pedro’s village in Mozambique was ravaged by floods. People were forced to higher grounds to avoid the floodwaters, and many people, including the heavily-pregnant Sofia Pedro, were climbed to shelter in the treetops. She was trapped in the tree for four days. On the third day, she gave birth to her daughter, Rositha.

Giving birth in the treetops is unusual for humans, but not for many primate species.

Stories like Sofia’s are particularly interesting because they pose the question: are humans unique in that they alone experience difficulties during birth? Do both human and nonhuman primates therefore adopt methods and strategies to minimize the risk and maximize survival of themselves and their offspring?

In other words, is there a gap in human and nonhuman primate parturition behavior?

To investigate the similarities and differences between human and nonhuman primate parturition strategies, one must examine 1.) the Anatomical characteristics to examine the physical difficulties humans and primates face when giving birth and 2.) Parturition strategies, in other words, how human and nonhuman primates manage birth and improve probability of survival of both the mother and infant.

Anatomical Characteristics 

The human and nonhuman birth canal divided into three transverse planes: the inlet, midplane, and outlet (fig. 1). Each plane is described as being either longest at either the anterior-posterior diameter or widest at the transverse diameter. Each plane may be aligned, meaning all three planes parallel to one another, or misaligned, the planes are perpendicular to one another, with the greatest diameter varying among the three planes

Figure 1. Pelvic inlet, midplane, and outlet

In the genus Pan birth canal, for example, the anterior-posterior diameter exceeds the transverse diameter. In Australopithecine (specifically A. aferensis) the pelvis inlet transverse diameter exceeds the anterior-posterior diameter, resulting in a platypelloid shape (i.e. a flat, oval shape). Among humans the three transverse are all misaligned; the inlet is widest transversely, and the outlet widest anterior-posteriorly; thus creating two perpendicular planes.

Figure 2. Comparison for the mechanism of birth in Pan, A.L. 288-1 (Australopithecus aferensis) and Homo (Tague and Lovejoy, 1986: 247)

The Australopithecine birth canal is an example of how useful it is to reconstruct and understand changes in birth and parturition among human and nonhuman primate ancestors.

Australopithecus serve as one of the earliest sources of fossil material for examining early human bipedalism, and for the purpose of this post, mechanisms of birth.  The cranial capacity of Australopithecus similar to that of modern chimpanzees. Pelvic and limb morphology indicate Australopithecines was bipedal, not but obligatory like our hominid ancestors. Australopithecines also had an increase in shoulder breadth co-occurs with bipedalism, helping with balance.

Australopithecine birth canal would have restricted fetal head rotations at all levels within the canal. Yet, the birth canal was adequate to allow passage of a neonate’s cranium only if the infant’s head entered with its occipital bone oriented transversely with ansynclitism, meaning the neonatal head tilted towards its left or right shoulder, and exited without rotating. The shoulders which followed probably would not have been able to pass through without changing orientation.

It is more difficult, if not impossible, to determine whether or not Australopithecines gave birth in solitude, among conspecifics, or sought attendants to assist with birth. Trevathan (1987) suggests that the presence of attendants at childbirth has been part of the genus heritage for at least one million to two million years, originating with encephalization in our linage. Hominid ancestors would have been able to give birth without assistance, but having that assistance and support would have made the difference between life and death for mothers and their infants. A slight reduction in mortality would lead to selection for the behavioral characteristic of seeking companionship during parturition, resulting in its widely universal distribution in the modern human species.

Anatomical Features of Human and Nonhuman Primate Birth

Sherwood Washburn referred to the human birth as the “obstetric dilemma,” resulting from the shrunken dimensions of the human birth canal mandated by the mechanical requirements of upright bipedal locomotion and the evolution of progressively larger human brains (Washburn, 1960). Among humans, the fetal head must be flexed as it passes underneath the subpubic arch/pubic symphysis, with the occiput against the pubic bones, the frontal bone passing along the concave anterior surface of the sacrum.  The infant’s head then emerges from the canal occiput anterior: meaning that the infant generally emerges from the birth canal facing the opposite direction from the mother.

Primate mechanism of parturition is slightly more difficult to investigate because observations and accounts of primate births in the wild are scarce. Primatologists who have observed primate births note the difficulties in differentiation between pregnant and non-pregnant females until the pregnant female is actually in labor. Also, some primates give birth nocturnally, thus lower the changes that they will be observed, and some even seclude themselves in the foliage of trees during parturition. Among greater apes, the spacious birth canal and large body size allow for the neonate to easily navigate the birth canal. Small-bodies primates and lesser apes (Ateles), proboscis monkeys (Nasalis), macaques (Macaca), and lesser apes or gibbions (Hylobates), have a smaller head-to-body proportions, thus potentially complicated the birthing process. In her PhD dissertation, Stoller (1995) examined radiographs of laboratory animals during parturition showed that squirrel monkey and baboon neonates entered the birth canal in various positions, but then rotate to exit face first, facing the maternal pubic bones with their heads in an extended position.

Human Primate Birthing Strategies 

Humans have adopted many strategies to combat the risks and difficulties in childbirth, one of which is seeking assistance from medical professionals or family members during the birth. Humans do have the ability to give birth without assistance, yet today many women giving birth prefer not to do it alone. Before the advent of modern obstetric care, pregnancy and childbirth were risky and dangerous, and the complex anatomical features involved in parturition predisposed humans to certain conditions, such as obstructed labor, which could result in a myriad of injuries to both the mother and infant (Roberts and Mancester, 2007; Arrowsmith et. al., 1996; Wall et. al., 2005). Thus, many women in developed societies view childbirth as an event to be managed with the presences of a trained professional using technological intervention (Liamputtong. 2007) to ensure that their pregnant bodies and fetuses are completely controlled, and therefore, safe (Liamputtong, 2007). To be sure there are benefits in having a trained medical professional present at the birth.

Obstructed births are a common complication humans face, one type in particular is shoulder dystocia, which occurs when the shoulders are unable to pass through the pelvis after delivery of the head when the neonate is too large and the pelvis too small. The typical medical intervention is a surgical incision to remove obstruction, which may be dangerous as it sometimes results in tearing or hemorrhaging, either of which might cause permanent damage or be fatal to the mother, infant, or both. Midwifes, on the other hand, adopt different strategies to combat shoulder dystocia: typically the maneuvers the parturent mother into different positions to widen the birth canal.

Birth positions in particular vary cross-culturally. Even though the semi-upright positions of kneeling and sitting are the best positions for parturition, the supine position is the most common in developed countries where birth typically occurs in a hospital. It is possible that many women do not have the stamina to remain in kneeling or sitting position for the length of time usually required to deliver a child. The supine position allows the medical professional to have optimal access to the birth canal as well. Interestingly, Friedman (1978) found that in general, the upright position is optimal for increasing intra-abdominal pressure and the diameter of the pelvis. Women who were upright in a seated or semi-reclined position during labor had a shorter labor length compared to women in a supine position (Friedman 1978).

Many women assign certain meanings to the birthing process; they feel a sense of achievement and pride in their ability to cope with intense pain. Mayan women living in Guatemala stated that they accept pain as an obligation of a woman’s life, and consider it a point of pride to confront the birth with stoic dignity and courage. In fact, the indigenous word for birth (patan) literally translates into “burden.”

Expressing and vocalizing any pain was, to some women, considered shameful because they believe such actions like screaming diverted energy needed to give birth. This is particularly true for Chinese women, who are also expected to use soft voices and demonstrate quiet demeanor during parturition.

Parturition Behaviors Among Nonhuman Primates 

Anatomically, it appears that the mechanism of parturition varies between primate species, specifically between large bodied and small-bodied apes. When scholars opine that primates have little to no problems during parturition, they do not consider the extrinsic challenges primates encounter when giving birth in their natural habitat. Observations of baboons reveals that females give birth among conspecific group members. Squirrel monkeys give birth within their group as well as a form of cooperation against predators, anti-predator vigilance, and defense of neonates. Among Chimpanzees, Goodall (1971) noted that pregnant females become more solitary as parturition approaches. Among some primates, females seek seclusion and take advantage of the tree foliage that provides a natural protection from terrestrial predators (Rosenberg and Trevathan 2002). In a study published in Primates in July 2014, primatologists observed a bonobo birth for the first time, and found that the parturent female was accompanied by two other females who, according the researchers, were “offering companionship and support.” After the birth, the mother as well as the so-called birth attendants all consumed the placenta.

Primate births may be diurnal verses nocturnal; in fact, primates give birth at times of day that offer the lowest predation risk. Among squirrel monkeys labor may being at dawn, and if the infant has not been birthed by daytime, labor will spontaneously stop and start again during the appropriate time, most likely during dusk.

Primates also maneuver into positions to widen pelvis, particularly among smaller-bodied primates with a very close caphalopelvic fit (e.g. macaca mullata). Primates also express pain when giving birth. Patas, Rhesus macaques, and bonobos have been observed having pained looks on faces and express said pain with vocalizations. Breeched births might occur among primates with a close cephalopelvic dimension, such as macaca mullata, rhesus macaques, spider monkeys.

So How Wide is the Parturition Gap?

The mechanism of birth appears to be more complex for humans, small-bodied primates, and lesser apes than compared to larger-bodied, greater apes. Humans opt to seek assistance during birth and while primates sometimes opt to give birth among group members, it is unclear whether or not primates actively seek birth attendants. Primates maneuver in positions optimal for birth while humans in medicalized cultures give birth in a less optimal, supine position; maybe humans should consider a primate model for birthing positions! Both human and nonhuman primates experience pain when giving birth, yet humans are unique in that they assign cultural meaning to their pain.

In sum, both face similar challenges when giving birth, yet the adaptive methods to overcome those challenges varies between species worldwide. It seems to be that the parturition gap between human and nonhuman primates is not a wide gap after all.

             

Sources:

Abitbol, M. (1996). Birth and Human Evlution; Anatomical and Obstertical Mechanics in Primates. Westpoint: Bergin & Garvey.

Abitbol, M. (1987). Obstetrics and psoture in pelvic anatomy. Journal of Human Evolution, 16, 243-256.

Arrowsmith, S., Hamlin, E., and Wall, L. (1996). “Obstructed labor injury complex”: obsteteric fistual formation and the mulitfaceted morbidity of maternal birth trauma in the developing world. Ostetrical and Gynecological Survey, 51, 568-574.

Berge, C. (1984). Obstetrical interpretation of the australopithecine pelvic cavity. Journal of Human Evolution, 13, 573-587.

Berge, C., and Ponge, J. (1983). Les caracteristiques de bassin des australopitheques (A. robustus, A. africanus, A. afarensis) sont elles licees a une bipedie de type humain?

Bulletins et Mémoires de la Société d’Anthropologie de Paris, 10, 335-354.

Berge, C., and R. Orban-Segebarth, P. S. (1984). Obstetrical Interpretation of the Australopithecine Pelvic Cavity. Journal of Human Evolution, 7, 573-587.

Boinski, S. (1987). Birth synchrony in squirrel monkeys (Saimiri oetstedi). Behavioral Ecology and Sociobiology, 21, 393-400.

Brandt, E., and Mitchell, G. (1971). Parturition in primates: behavior related to birth. In Primate Behavior: Developments in Field and Laboratory Research L. Rosenblum (Ed.), (Vol. 2, pp. 177-223). New York: Academic Press.

Chism, J., Olson, D., and Rowell, T. (1983). Diurnal Births and Perinatal Behavior Among Wild Patas Monkeys: Evidence of an Adaptive Pattern. International Journal of Primatology, 4(2), 167-184.

Clark, L., Khalaf, I., Semenic, S., Kartchner, R., and K.Vehvilainen-Julkunen. (2003). The Pain of Childbirth: Perceptions of Cultually Diverse Women. Pain Management Nursing, 4(4), 145-154.

DeSilva, J., and Lesnik, J. (2008). Brain size at birth throughout human evolution: A new method for estimating neonatal brain size in hominins. Journal of Human Evolution, 55, 1064-1074.

Dunbar, R.I.M. and Dunbar, P. (1974). Behavior related to birth in wild gelada baboons (Theropithecus gelada). Behavior, 185-191.

Friedman, E. (1978). Labor: Clinical Evaluation and Management. New York: Appleton-Century-Crofts.

Goodall, J. (1971). In the Shadow of Man. New York: Dell.

Gorzitze, A. (1996). Birth-related Behaviors in Wild Proboscis. Primates , 37 (1), 75-78.

Hausler, M., and Schmid, P. (1995). Comparisons of the pelves of Sts 14 and Al 288-1: implications for birth and sexual dimorphism in australopithecines. Journal of Human Evolution, 29, 363-383.

Hopf, S. (1967). Notes on pregnancy, delivery and infant survival in captive squirrel monkeys. Primates, 8, 323-332.

Kadam, K., and Swayamprabha, M. (1980). Parturition in the slender loris (Loris tardigradus lydekkerianus). Primates, 21, 567-571.

Kibii, J., Churchill, S., Schmid, P., Carlson, K., Reed, N., de Ruiter, D., et al. (2011). A Partial Pelvis of Australopithecus sediba. Science, 333, 1407-1411.

Kummer, H. (1968). Social Organization of Hamadryas Baboons. Basel: Karger.

Leaky, M., Feibel, C., McDougall, I., & Walker, A. (1995). New four-million-year-old hominidspecies from Kanapoi and Allia Bay, Kenya. Nature , 376, 565-571.

Lefebvre, L., and Carli, G. (1985). Parturition in Non-Human Primates: Pain and Auditory Concealment. Pain , 21, 315-327.

Likens, E. (2013). Resolving Shoulder Dystocia: Is Episiotomy Best Practice? Midwifery Today, 44-45.

Lipscomb, K. (1994). Shoulder dystocia. In D. M. Brenner (Ed.), Management of Common Problems in Obstertrics and Gynecology (pp. 227-232). London: Blackwell Scientific.

McKenna, J. (1974). Perinatal behavior and parturition of a Colobinae Presbytis entellus entullus (hanuman langur). Lab. Primate Newsletter, 13, 13-15.

Mir, S., & Ahmad, A. (2010). Shoulder Dystocia. Journal of Medical Education and Research, 12 (4), 165-167.

Oppenheimer, J. (1976). Presbytis entellus: Birth in free-ranging primate troop. Primates, 17, 541-542.

Rawal, J., Shah, A., Stirk, F., & Mehtar, S. (1994). Water birth and infection in babies. British Medical Journal , 309, 511.

Roberts, C., & Mancester, K. (2007). The Archaeology of Disease. Ithaca: Cornell University Press.

Rosenberg, K. (1992). The evolution of modern human childbirth. Yearbook of Physical Anthropology, 35, 89-124.

Rosenberg, K. and Trevathan, W. (2001). The Evolution of Human Birth. Scientific American, 285(5), 72-71

Rosenberg, K., and Trevathan, W. (2002). Birth, obstetrics and human evolution. International Journal of Obsterics and Gynaecology, 109, 1199-1206.

Ruff, C. (1995). Biomechanics of the hip and birth in early Homo. American Journal of Physical Anthropology, 98, 527-574.

Schultz, A. (1949). Sex differences in the pelves of primates. American Journal of Physical Anthropology, 7, 401-423.

Sekulic, R. (1982). Birth in free-ranging howler monkeys Alouatta seniculus. Primates, 23, 580-582.

Smeltzer, A. (1986). Prevention and management of shoulder dystocia. Clinical Obstetrics and Gynecology, 29, 299-308.

Stoller, M. (1995). The obstetric pelvis and mechanism of labor in nonhuman primates. [PhD dissertation]. University of Chicago.

Strum, S., and Fedigan, L. (2000). Changing Views of Primate Society. In Primate Encounters (pp. 3-49). S. Strum, & L. Fedigan (Eds.), Chicago and London: University of Chicago Press.

Suzuki, M., T. Ono, M. K., and Cho, F. (1990). Hour of Delivery in Cynomolgus Monkeys Under Indoor Individually-caged Conditions. Primates, 31 (2), 215-255.

Tague, R., and Lovejoy, C. (1998). A. L. 288-1—Lucy or Lucifer: gender confusion in the Pliocene. Journal of Human Evolution, 35(1), 75-94.

Tague, R., and Lovejoy, C. (1986). The Obstetric Pelvis of A.L. 288-1 (Lucy). Journal of Human Evolution, 15, 237-255.

Takeshita, H. (1961-1962). On the delivery behavior of squirrel monkeys (Saimiri sciurea) and a mona monkey (Ceropithecus mona). Primates, 3(1), 59-72.

Tinklepaugh, O., and Hartman, C. (1930). Behavioral aspects of parturition in the monkey (Macascas rhesus). Comparative Psychology 11, 63-98.

Trevathan, W. (1988). Fetal emergence patterns in evolutionary perspective. American Anthropology, 90, 674-681.

Trevathan, W. (1987). Human Birth: An Evolutionary Perspective . New York: Aldine de Gruyter.

Trevathan, W. (2003). The evolution of bipedalism and assisted birth. Medical Anthropology Quarterly, 10, 287-298.

Trevathan, W., and Rosenberg, K. (2000). The shoulders follow the head: postcranial constraints on human childbirth. Journal of Human Evolution , 39, 583-586.

Wall, L., Arrowsmith, S., and Briggs, N. (2005). The obstetric vesicovaginal fistula in the developing world. Obstetrical Gynecological Survey, 60, S1-S55.

Ward, C. (2002). Interpreting the posture and locomotion of Australopithecus afarensis: where do we stand?. Yearbook of Physical Anthropology, 45, 185-215.

Washbum, S. (1960). Tools and human evolution. Scientific American, 203, 3-15.

White, T. (2000). Human Osteology. San Diego: Academic Press.

Wittman, A., & Wall, L. (2007). The Evolutionary Origins of Obstructed Labor: Bipedalism, Encephalization, and the Human Obstetric Dilemma. Obstetrical and Gynecological Survey, 62 (11), 739-748.

Wolpoff, M. (1999). Paleoanthropology. Boston: McGraw-Hill.